diff --git a/cli/types/cypress.d.ts b/cli/types/cypress.d.ts
index 6611f3ec08ef..65f51f96722e 100644
--- a/cli/types/cypress.d.ts
+++ b/cli/types/cypress.d.ts
@@ -1826,11 +1826,6 @@ declare namespace Cypress {
      */
     prevUntil<E extends Node = HTMLElement>(element: E | JQuery<E>, filter?: string, options?: Partial<Loggable & Timeoutable>): Chainable<JQuery<E>>
 
-    /**
-     * TODO: add docs
-     */
-    prompt(message: string, options?: Partial<Loggable & Timeoutable>): Chainable<Subject>
-
     /**
      * Read a file and yield its contents.
      *
@@ -3163,11 +3158,6 @@ declare namespace Cypress {
      * @default false
      */
     experimentalStudio: boolean
-    /**
-     * Enables the prompt command feature.
-     * @default false
-     */
-    experimentalPromptCommand: boolean
     /**
      * Adds support for testing in the WebKit browser engine used by Safari. See https://on.cypress.io/webkit-experiment for more information.
      * @default false
diff --git a/packages/app/src/runner/event-manager.ts b/packages/app/src/runner/event-manager.ts
index 109f9f4aae19..3cecac6f6f1d 100644
--- a/packages/app/src/runner/event-manager.ts
+++ b/packages/app/src/runner/event-manager.ts
@@ -798,21 +798,7 @@ export class EventManager {
       },
     )
 
-    /**
-     * Call a backend request for the requesting spec bridge since we cannot have websockets in the spec bridges.
-     * Return it's response.
-     */
-    Cypress.primaryOriginCommunicator.on('backend:request', async ({ args }, { source, responseEvent }) => {
-      let response
-
-      try {
-        response = await Cypress.backend(...args)
-      } catch (error) {
-        response = { error }
-      }
-
-      Cypress.primaryOriginCommunicator.toSource(source, responseEvent, response)
-    })
+    Cypress.handlePrimaryOriginSocketEvent(Cypress, 'backend:request')
 
     /**
      * Call an automation request for the requesting spec bridge since we cannot have websockets in the spec bridges.
diff --git a/packages/driver/cypress.config.ts b/packages/driver/cypress.config.ts
index d7df5cbee75b..f67b3467effa 100644
--- a/packages/driver/cypress.config.ts
+++ b/packages/driver/cypress.config.ts
@@ -7,6 +7,7 @@ export const baseConfig: Cypress.ConfigOptions = {
   experimentalStudio: true,
   experimentalMemoryManagement: true,
   experimentalWebKitSupport: true,
+  // @ts-expect-error - this will not error when we actually release the experimentalPromptCommand flag
   experimentalPromptCommand: true,
   hosts: {
     'foobar.com': '127.0.0.1',
diff --git a/packages/driver/cypress/e2e/commands/prompt.cy.ts b/packages/driver/cypress/e2e/commands/prompt.cy.ts
index 78ba0620c4bc..7f5e1cc0af1e 100644
--- a/packages/driver/cypress/e2e/commands/prompt.cy.ts
+++ b/packages/driver/cypress/e2e/commands/prompt.cy.ts
@@ -7,10 +7,18 @@ describe('src/cy/commands/prompt', () => {
       return
     }
 
-    cy.visit('/fixtures/dom.html')
+    cy.visit('http://www.foobar.com:3500/fixtures/dom.html')
 
     // TODO: add more tests when cy.prompt is built out, but for now this just
     // verifies that the command executes without throwing an error
+    // @ts-expect-error - this will not error when we actually release the experimentalPromptCommand flag
     cy.prompt('Hello, world!')
+
+    cy.visit('http://www.barbaz.com:3500/fixtures/dom.html')
+
+    cy.origin('http://www.barbaz.com:3500', () => {
+      // @ts-expect-error - this will not error when we actually release the experimentalPromptCommand flag
+      cy.prompt('Hello, world!')
+    })
   })
 })
diff --git a/packages/driver/cypress/e2e/e2e/origin/patches.cy.ts b/packages/driver/cypress/e2e/e2e/origin/patches.cy.ts
index 2bdc0fbdb6b3..f1d62636dc91 100644
--- a/packages/driver/cypress/e2e/e2e/origin/patches.cy.ts
+++ b/packages/driver/cypress/e2e/e2e/origin/patches.cy.ts
@@ -63,7 +63,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     describe('from the AUT', () => {
       beforeEach(() => {
         cy.intercept('/test-request').as('testRequest')
-        cy.stub(Cypress, 'backend').log(false).callThrough()
+        cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
 
         cy.visit('/fixtures/primary-origin.html')
         cy.get('a[data-cy="xhr-fetch-requests"]').click()
@@ -87,7 +87,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
 
               cy.wait('@testRequest')
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -107,7 +107,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
 
               cy.wait('@testRequest')
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -127,7 +127,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
 
               cy.wait('@testRequest')
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -152,7 +152,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           )
 
           cy.then(() => {
-            expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+            expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
           })
         })
 
@@ -171,7 +171,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           )
 
           cy.then(() => {
-            expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+            expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
               url: 'http://app.foobar.com:3500/test-request',
               resourceType: 'fetch',
               credentialStatus: 'include',
@@ -184,7 +184,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     describe('from the spec bridge', () => {
       beforeEach(() => {
         cy.intercept('/test-request').as('testRequest')
-        cy.stub(Cypress, 'backend').log(false).callThrough()
+        cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
 
         cy.visit('/fixtures/primary-origin.html')
         cy.get('a[data-cy="xhr-fetch-requests"]').click()
@@ -216,7 +216,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
               })
 
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request-credentials',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -246,7 +246,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
               })
 
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request-credentials',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -274,7 +274,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
               })
 
               cy.then(() => {
-                expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+                expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                   url: 'http://www.foobar.com:3500/test-request-credentials',
                   resourceType: 'fetch',
                   credentialStatus: assertCredentialStatus,
@@ -297,7 +297,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
             })
 
           cy.then(() => {
-            expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+            expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
           })
         })
       })
@@ -326,7 +326,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           })
 
         cy.then(() => {
-          expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+          expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
             url: 'http://app.foobar.com:3500/test-request',
             resourceType: 'fetch',
             credentialStatus: 'include',
@@ -339,13 +339,13 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
       // manually remove the spec bridge iframe to ensure Cypress.state('window') is not already set
       window.top?.document.getElementById('Spec\ Bridge:\ foobar.com')?.remove()
 
-      cy.stub(Cypress, 'backend').log(false).callThrough()
+      cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
 
       cy.visit('/fixtures/primary-origin.html')
       cy.get('a[data-cy="xhr-fetch-requests-onload"]').click()
 
       cy.then(() => {
-        expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+        expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
           url: 'http://localhost:3500/foo.bar.baz.json',
           resourceType: 'fetch',
           credentialStatus: 'same-origin',
@@ -354,7 +354,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     })
 
     it('does not patch fetch in the spec window or the AUT if the AUT is on the primary', () => {
-      cy.stub(Cypress, 'backend').log(false).callThrough()
+      cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
       cy.visit('fixtures/xhr-fetch-requests.html')
 
       cy.window().then((win) => {
@@ -371,14 +371,14 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
       cy.then(async () => {
         await fetch('/test-request')
 
-        expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+        expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('request:sent:with:credentials')
       })
 
       // expect AUT to NOT be patched in primary
       cy.window().then(async (win) => {
         await win.fetch('/test-request')
 
-        expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+        expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('request:sent:with:credentials')
       })
     })
   })
@@ -387,7 +387,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     describe('from the AUT', () => {
       beforeEach(() => {
         cy.intercept('/test-request').as('testRequest')
-        cy.stub(Cypress, 'backend').log(false).callThrough()
+        cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
 
         cy.visit('/fixtures/primary-origin.html')
         cy.get('a[data-cy="xhr-fetch-requests"]').click()
@@ -409,7 +409,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
 
             cy.wait('@testRequest')
             cy.then(() => {
-              expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+              expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                 url: 'http://www.foobar.com:3500/test-request',
                 resourceType: 'xhr',
                 credentialStatus: withCredentials,
@@ -431,7 +431,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
             })
 
           cy.then(() => {
-            expect(Cypress.backend).to.have.been.calledWithMatch('request:sent:with:credentials')
+            expect(Cypress.backendRequestHandler).to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
           })
         })
       })
@@ -449,7 +449,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           })
 
         cy.then(() => {
-          expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+          expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
             url: 'http://app.foobar.com:3500/test-request',
             resourceType: 'xhr',
             credentialStatus: true,
@@ -461,9 +461,9 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     describe('from the spec bridge', () => {
       beforeEach(() => {
         cy.intercept('/test-request').as('testRequest')
-        cy.stub(Cypress, 'backend').log(false).callThrough()
+        cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
         cy.origin('http://www.foobar.com:3500', () => {
-          cy.stub(Cypress, 'backend').log(false).callThrough()
+          cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
         })
 
         cy.visit('/fixtures/primary-origin.html')
@@ -501,7 +501,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
             })
 
             cy.then(() => {
-              expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+              expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
                 url: 'http://www.foobar.com:3500/test-request-credentials',
                 resourceType: 'xhr',
                 credentialStatus: withCredentials,
@@ -523,7 +523,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
             })
 
           cy.then(() => {
-            expect(Cypress.backend).to.have.been.calledWithMatch('request:sent:with:credentials')
+            expect(Cypress.backendRequestHandler).to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
           })
         })
 
@@ -553,7 +553,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
             })
 
           cy.then(() => {
-            expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+            expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
               url: 'http://app.foobar.com:3500/test-request',
               resourceType: 'xhr',
               credentialStatus: true,
@@ -567,13 +567,13 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
       // manually remove the spec bridge iframe to ensure Cypress.state('window') is not already set
       window.top?.document.getElementById('Spec\ Bridge:\ foobar.com')?.remove()
 
-      cy.stub(Cypress, 'backend').log(false).callThrough()
+      cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
 
       cy.visit('/fixtures/primary-origin.html')
       cy.get('a[data-cy="xhr-fetch-requests-onload"]').click()
 
       cy.then(() => {
-        expect(Cypress.backend).to.have.been.calledWith('request:sent:with:credentials', {
+        expect(Cypress.backendRequestHandler).to.have.been.calledWith('backend:request', 'request:sent:with:credentials', {
           url: 'http://localhost:3500/foo.bar.baz.json',
           resourceType: 'xhr',
           credentialStatus: false,
@@ -582,7 +582,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
     })
 
     it('does not patch xmlHttpRequest in the spec window or the AUT if the AUT is on the primary', () => {
-      cy.stub(Cypress, 'backend').log(false).callThrough()
+      cy.stub(Cypress, 'backendRequestHandler').log(false).callThrough()
       cy.visit('fixtures/xhr-fetch-requests.html')
 
       cy.window().then((win) => {
@@ -614,7 +614,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           xhr.send()
         })
 
-        expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+        expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
       })
 
       // expect AUT to NOT be patched in primary
@@ -636,7 +636,7 @@ describe('src/cross-origin/patches', { browser: '!webkit', defaultCommandTimeout
           xhr.send()
         })
 
-        expect(Cypress.backend).not.to.have.been.calledWithMatch('request:sent:with:credentials')
+        expect(Cypress.backendRequestHandler).not.to.have.been.calledWithMatch('backend:request', 'request:sent:with:credentials')
       })
     })
   })
diff --git a/packages/driver/package.json b/packages/driver/package.json
index 74e6d84bb986..1f764d7701cd 100644
--- a/packages/driver/package.json
+++ b/packages/driver/package.json
@@ -53,6 +53,7 @@
     "chai-subset": "1.6.0",
     "clone": "2.1.2",
     "common-tags": "1.8.0",
+    "component-emitter": "1.3.0",
     "compression": "1.8.0",
     "cookie-parser": "1.4.5",
     "core-js-pure": "3.21.0",
diff --git a/packages/driver/src/cross-origin/communicator.ts b/packages/driver/src/cross-origin/communicator.ts
index 550a6955f79c..32564b8c2234 100644
--- a/packages/driver/src/cross-origin/communicator.ts
+++ b/packages/driver/src/cross-origin/communicator.ts
@@ -336,7 +336,7 @@ export class SpecBridgeCommunicator extends EventEmitter {
   }: {
     event: string
     data?: Cypress.ObjectLike
-    options: {syncGlobals: boolean}
+    options?: {syncGlobals: boolean}
     timeout: number
   }) {
     return new Promise<T>((resolve, reject) => {
diff --git a/packages/driver/src/cross-origin/cypress.ts b/packages/driver/src/cross-origin/cypress.ts
index c6af33aad03c..64a0aca56c9f 100644
--- a/packages/driver/src/cross-origin/cypress.ts
+++ b/packages/driver/src/cross-origin/cypress.ts
@@ -14,7 +14,7 @@ import { bindToListeners } from '../cy/listeners'
 import { handleOriginFn } from './origin_fn'
 import { FINAL_SNAPSHOT_NAME } from '../cy/snapshots'
 import { handleLogs } from './events/logs'
-import { handleSocketEvents } from './events/socket'
+import { handleCrossOriginSocketEvent, handleDefaultCrossOriginSocketEvents } from './events/socket'
 import { handleSpecWindowEvents } from './events/spec_window'
 import { handleErrorEvent } from './events/errors'
 import { handleScreenshots } from './events/screenshots'
@@ -120,6 +120,12 @@ const setup = ({ cypressConfig, env, isProtocolEnabled }: { cypressConfig: Cypre
 
   const { state, config } = Cypress
 
+  // These need to happen before the commands are created so that commands can
+  // use things like Cypress.backend during their creation.
+  handleDefaultCrossOriginSocketEvents(Cypress)
+
+  Cypress.handleCrossOriginSocketEvent = handleCrossOriginSocketEvent
+
   // @ts-ignore
   Cypress.Commands = $Commands.create(Cypress, cy, state, config)
   // @ts-ignore
@@ -141,7 +147,6 @@ const setup = ({ cypressConfig, env, isProtocolEnabled }: { cypressConfig: Cypre
 
   handleOriginFn(Cypress, cy)
   handleLogs(Cypress)
-  handleSocketEvents(Cypress)
   handleSpecWindowEvents(cy)
   handleMiscEvents(Cypress, cy)
   handleScreenshots(Cypress)
diff --git a/packages/driver/src/cross-origin/events/socket.ts b/packages/driver/src/cross-origin/events/socket.ts
index a159e1ea5554..3cc996a71e54 100644
--- a/packages/driver/src/cross-origin/events/socket.ts
+++ b/packages/driver/src/cross-origin/events/socket.ts
@@ -1,20 +1,24 @@
-export const handleSocketEvents = (Cypress) => {
-  const onRequest = async (event, args) => {
-    // The last argument is the callback, pop that off before messaging primary and call it with the response.
-    const callback = args.pop()
-    const response = await Cypress.specBridgeCommunicator.toPrimaryPromise({
-      event,
-      data: { args },
-      timeout: Cypress.config().defaultCommandTimeout,
-    })
+const onRequest = async (event, args) => {
+  // The last argument is the callback, pop that off before messaging primary and call it with the response.
+  const callback = args.pop()
+  const response = await Cypress.specBridgeCommunicator.toPrimaryPromise<{ error?: string, response?: any }>({
+    event,
+    data: { args },
+    timeout: Cypress.config().defaultCommandTimeout,
+  })
 
-    if (response && response.error) {
-      return callback({ error: response.error })
-    }
-
-    callback({ response })
+  if (response && response.error) {
+    return callback({ error: response.error })
   }
 
-  Cypress.on('backend:request', (...args) => onRequest('backend:request', args))
-  Cypress.on('automation:request', (...args) => onRequest('automation:request', args))
+  callback({ response })
+}
+
+export const handleCrossOriginSocketEvent = (Cypress, eventName: string) => {
+  Cypress.on(eventName, (...args) => onRequest(eventName, args))
+}
+
+export const handleDefaultCrossOriginSocketEvents = (Cypress) => {
+  handleCrossOriginSocketEvent(Cypress, 'backend:request')
+  handleCrossOriginSocketEvent(Cypress, 'automation:request')
 }
diff --git a/packages/driver/src/cy/commands/prompt/index.ts b/packages/driver/src/cy/commands/prompt/index.ts
index 96d00215a12e..65c52ec93acb 100644
--- a/packages/driver/src/cy/commands/prompt/index.ts
+++ b/packages/driver/src/cy/commands/prompt/index.ts
@@ -1,15 +1,24 @@
 import { init, loadRemote } from '@module-federation/runtime'
-import type{ CyPromptDriverDefaultShape } from './prompt-driver-types'
+import type { CypressInternal, CyPromptDriverDefaultShape } from './prompt-driver-types'
+import type Emitter from 'component-emitter'
 
 interface CyPromptDriver { default: CyPromptDriverDefaultShape }
 
-let initializedCyPrompt: CyPromptDriverDefaultShape | null = null
-const initializeCloudCyPrompt = async (Cypress: Cypress.Cypress): Promise<CyPromptDriverDefaultShape> => {
+declare global {
+  interface Window {
+    getEventManager?: () => {
+      ws: Emitter
+    }
+  }
+}
+
+let initializedModule: CyPromptDriverDefaultShape | null = null
+const initializeModule = async (Cypress: Cypress.Cypress, cy: Cypress.Cypress['cy']): Promise<CyPromptDriverDefaultShape> => {
   // Wait for the cy prompt bundle to be downloaded and ready
   const { success } = await Cypress.backend('wait:for:cy:prompt:ready')
 
   if (!success) {
-    throw new Error('CyPromptDriver not found')
+    throw new Error('error waiting for cy prompt bundle to be downloaded and ready')
   }
 
   // Once the cy prompt bundle is downloaded and ready,
@@ -31,35 +40,48 @@ const initializeCloudCyPrompt = async (Cypress: Cypress.Cypress): Promise<CyProm
   const module = await loadRemote<CyPromptDriver>('cy-prompt')
 
   if (!module?.default) {
-    throw new Error('CyPromptDriver not found')
+    throw new Error('error loading cy prompt driver')
   }
 
-  initializedCyPrompt = module.default
+  initializedModule = module.default
+
+  return initializedModule
+}
+
+const initializeCloudCyPrompt = async (Cypress: Cypress.Cypress, cy: Cypress.Cypress['cy']) => {
+  let cloudModule = initializedModule
 
-  return module.default
+  if (!cloudModule) {
+    cloudModule = await initializeModule(Cypress, cy)
+  }
+
+  return cloudModule.createCyPrompt({
+    Cypress: Cypress as CypressInternal,
+    cy,
+    eventManager: window.getEventManager ? window.getEventManager() : undefined,
+  })
 }
 
 export default (Commands, Cypress, cy) => {
   if (Cypress.config('experimentalPromptCommand')) {
+    let initializeCloudCyPromptPromise: Promise<ReturnType<CyPromptDriverDefaultShape['createCyPrompt']>> | undefined
+
+    if (Cypress.browser.family === 'chromium' || Cypress.browser.name === 'electron') {
+      initializeCloudCyPromptPromise = initializeCloudCyPrompt(Cypress, cy)
+    }
+
     Commands.addAll({
-      async prompt (message: string) {
-        if (Cypress.browser.family !== 'chromium' && Cypress.browser.name !== 'electron') {
+      async prompt (message: string, options: object = {}) {
+        if (!initializeCloudCyPromptPromise) {
           // TODO: (cy.prompt) We will look into supporting other browsers (and testing them)
           // as this is rolled out
           throw new Error('`cy.prompt()` is not supported in this browser.')
         }
 
         try {
-          let cloud = initializedCyPrompt
-
-          // If the cy prompt driver is not initialized,
-          // we need to wait for it to be initialized
-          // before using it
-          if (!cloud) {
-            cloud = await initializeCloudCyPrompt(Cypress)
-          }
+          const cyPrompt = await initializeCloudCyPromptPromise
 
-          return await cloud.cyPrompt(Cypress, message)
+          return await cyPrompt(message, options)
         } catch (error) {
           // TODO: handle this better
           throw new Error(`CyPromptDriver not found: ${error}`)
diff --git a/packages/driver/src/cy/commands/prompt/prompt-driver-types.ts b/packages/driver/src/cy/commands/prompt/prompt-driver-types.ts
index 3f742f4b9678..2b57f796ce6b 100644
--- a/packages/driver/src/cy/commands/prompt/prompt-driver-types.ts
+++ b/packages/driver/src/cy/commands/prompt/prompt-driver-types.ts
@@ -1,7 +1,55 @@
-export interface CypressInternal extends Cypress.Cypress {
-  backend: (eventName: string, ...args: any[]) => Promise<any>
+import type Emitter from 'component-emitter'
+
+interface InternalActions extends Cypress.Actions {
+  (
+    eventName: 'prompt:backend:request',
+    listener: (...args: any[]) => void
+  ): Cypress.Cypress
+}
+
+export interface CypressInternalBase extends Cypress.Cypress {
+  backendRequestHandler: (
+    backendRequestNamespace: string,
+    eventName: string,
+    ...args: any[]
+  ) => Promise<any>
+  on: InternalActions
+}
+
+interface CrossOriginCypressInternal extends CypressInternalBase {
+  isCrossOriginSpecBridge: true
+  handleCrossOriginSocketEvent: (
+    Cypress: CypressInternal,
+    eventName: string
+  ) => void
+}
+
+interface SameOriginCypressInternal extends CypressInternalBase {
+  isCrossOriginSpecBridge: false
+  handlePrimaryOriginSocketEvent: (
+    Cypress: CypressInternal,
+    eventName: string
+  ) => void
+}
+
+export type CypressInternal =
+  | CrossOriginCypressInternal
+  | SameOriginCypressInternal
+
+export interface CyPromptEventManager {
+  ws: Emitter
+}
+
+export interface CyPromptOptions {
+  Cypress: CypressInternal
+  cy: Cypress.cy
+  // Note that the eventManager is present in same origin AUTs, but not cross origin
+  // so we need to check for it's presence before using it
+  eventManager?: CyPromptEventManager
 }
 
 export interface CyPromptDriverDefaultShape {
-  cyPrompt: (Cypress: CypressInternal, text: string) => Promise<void>
+  createCyPrompt: (
+    options: CyPromptOptions
+  ) => (text: string, commandOptions?: object) => Promise<void>
 }
diff --git a/packages/driver/src/cypress.ts b/packages/driver/src/cypress.ts
index c8657904fae7..dd7e47d887d9 100644
--- a/packages/driver/src/cypress.ts
+++ b/packages/driver/src/cypress.ts
@@ -88,6 +88,31 @@ interface AutomationError extends Error {
 // Are we running Cypress in Cypress? (Used for E2E Testing for Cypress in Cypress only)
 const isCypressInCypress = document.defaultView !== top
 
+const handlePrimaryOriginSocketEvent = (Cypress, backendRequestNamespace: string) => {
+  Cypress.primaryOriginCommunicator.on(
+    backendRequestNamespace,
+    async ({ args: [eventName, ...args] }: { args: [string, any[]] }, { source, responseEvent }) => {
+      let response
+
+      try {
+        response = await Cypress.backendRequestHandler(
+          backendRequestNamespace,
+          eventName,
+          ...args,
+        )
+      } catch (error) {
+        response = { error }
+      }
+
+      Cypress.primaryOriginCommunicator.toSource(
+        source,
+        responseEvent,
+        response,
+      )
+    },
+  )
+}
+
 class $Cypress {
   cy: any
   chai: any
@@ -161,6 +186,8 @@ class $Cypress {
   sinon = sinon
   lolex = fakeTimers
 
+  handlePrimaryOriginSocketEvent = handlePrimaryOriginSocketEvent
+
   static $: any
   static utils: any
 
@@ -764,7 +791,7 @@ class $Cypress {
     }
   }
 
-  backend (eventName, ...args) {
+  backendRequestHandler (backendRequestNamespace: string, eventName, ...args) {
     return new Promise((resolve, reject) => {
       const fn = function (reply) {
         const e = reply.error
@@ -787,10 +814,14 @@ class $Cypress {
         return resolve(reply.response)
       }
 
-      return this.emit('backend:request', eventName, ...args, fn)
+      return this.emit(backendRequestNamespace, eventName, ...args, fn)
     })
   }
 
+  backend (eventName, ...args) {
+    return this.backendRequestHandler('backend:request', eventName, ...args)
+  }
+
   automation (eventName, ...args) {
     // wrap action in promise
     return new Promise((resolve, reject) => {
diff --git a/packages/driver/types/internal-types-lite.d.ts b/packages/driver/types/internal-types-lite.d.ts
index c41aef97cf6a..0c1a809653ba 100644
--- a/packages/driver/types/internal-types-lite.d.ts
+++ b/packages/driver/types/internal-types-lite.d.ts
@@ -11,7 +11,9 @@ declare namespace Cypress {
     primaryOriginCommunicator: import('eventemitter2').EventEmitter2 & {
       toSpecBridge: (origin: string, event: string, data?: any, responseEvent?: string) => void
       userInvocationStack?: string
+      toSource: (source: string, responseEvent: string, response: any) => void
     }
+    backendRequestHandler: (backendRequestNamespace: string, emitter: Emitter, eventName: string, ...args: any[]) => Promise<any>
   }
 
   interface Actions {
diff --git a/packages/driver/types/internal-types.d.ts b/packages/driver/types/internal-types.d.ts
index bc632521e2b2..4794fca9cfbe 100644
--- a/packages/driver/types/internal-types.d.ts
+++ b/packages/driver/types/internal-types.d.ts
@@ -53,6 +53,7 @@ declare namespace Cypress {
     utils: CypressUtils
     events: Events
     specBridgeCommunicator: import('../src/cross-origin/communicator').SpecBridgeCommunicator
+    handleCrossOriginSocketEvent?: typeof handleCrossOriginSocketEvent
     mocha: $Mocha
     configure: (config: Cypress.ObjectLike) => void
     isCrossOriginSpecBridge: boolean
diff --git a/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts b/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
index c3d08058b4d6..aa9bb17b0cf8 100644
--- a/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
+++ b/packages/server/lib/cloud/cy-prompt/CyPromptManager.ts
@@ -2,6 +2,7 @@ import type { CyPromptManagerShape, CyPromptStatus, CyPromptServerDefaultShape,
 import type { Router } from 'express'
 import Debug from 'debug'
 import { requireScript } from '../require_script'
+import type { Socket } from 'socket.io'
 
 interface CyPromptServer { default: CyPromptServerDefaultShape }
 
@@ -38,9 +39,9 @@ export class CyPromptManager implements CyPromptManagerShape {
     }
   }
 
-  async handleBackendRequest (eventName: string, ...args: any[]): Promise<any> {
+  addSocketListeners (socket: Socket): void {
     if (this._cyPromptServer) {
-      return this.invokeAsync('handleBackendRequest', { isEssential: false }, eventName, ...args)
+      this.invokeSync('addSocketListeners', { isEssential: true }, socket)
     }
   }
 
@@ -89,6 +90,7 @@ export class CyPromptManager implements CyPromptManagerShape {
     }
 
     try {
+      // @ts-expect-error - TS not associating the method & args properly, even though we know it's correct
       return await this._cyPromptServer[method].apply(this._cyPromptServer, args)
     } catch (error: unknown) {
       let actualError: Error
diff --git a/packages/server/lib/project-base.ts b/packages/server/lib/project-base.ts
index 222201d23c59..29db121758a6 100644
--- a/packages/server/lib/project-base.ts
+++ b/packages/server/lib/project-base.ts
@@ -158,6 +158,7 @@ export class ProjectBase extends EE {
     process.chdir(this.projectRoot)
 
     this._server = new ServerBase(cfg)
+    // @ts-expect-error - this will not error when we actually release the experimentalPromptCommand flag
     if (cfg.experimentalPromptCommand) {
       const cyPromptLifecycleManager = new CyPromptLifecycleManager()
 
diff --git a/packages/server/lib/socket-base.ts b/packages/server/lib/socket-base.ts
index aa254b2e4285..810a6ab643b3 100644
--- a/packages/server/lib/socket-base.ts
+++ b/packages/server/lib/socket-base.ts
@@ -23,7 +23,7 @@ import type { Automation } from './automation'
 // eslint-disable-next-line no-duplicate-imports
 import type { Socket } from '@packages/socket'
 
-import type { RunState, CachedTestState, ProtocolManagerShape, AutomationCommands, CyPromptManagerShape } from '@packages/types'
+import type { RunState, CachedTestState, ProtocolManagerShape, AutomationCommands } from '@packages/types'
 import memory from './browsers/memory'
 import { privilegedCommandsManager } from './privileged-commands/privileged-commands-manager'
 
@@ -412,6 +412,10 @@ export class SocketBase {
           studio.addSocketListeners(socket)
         })
 
+        getCtx().coreData.cyPromptLifecycleManager?.registerCyPromptReadyListener((cyPrompt) => {
+          cyPrompt.addSocketListeners(socket)
+        })
+
         socket.on('studio:init', async (cb) => {
           try {
             const { canAccessStudioAI } = await options.onStudioInit()
@@ -449,12 +453,6 @@ export class SocketBase {
           }
         })
 
-        let cyPrompt: CyPromptManagerShape | undefined
-
-        getCtx().coreData.cyPromptLifecycleManager?.registerCyPromptReadyListener((cp) => {
-          cyPrompt = cp
-        })
-
         socket.on('backend:request', (eventName: string, ...args) => {
           const userAgent = socket.request?.headers['user-agent'] || getCtx().coreData.app.browserUserAgent
 
@@ -464,10 +462,6 @@ export class SocketBase {
           debug('backend:request %o', { eventName, args })
 
           const backendRequest = () => {
-            if (eventName.startsWith('cy:prompt:')) {
-              return cyPrompt?.handleBackendRequest(eventName, ...args)
-            }
-
             switch (eventName) {
               case 'preserve:run:state':
                 runState = args[0]
diff --git a/packages/server/test/support/fixtures/cloud/cy-prompt/test-cy-prompt.ts b/packages/server/test/support/fixtures/cloud/cy-prompt/test-cy-prompt.ts
index cde602ab31ff..0eea3553260d 100644
--- a/packages/server/test/support/fixtures/cloud/cy-prompt/test-cy-prompt.ts
+++ b/packages/server/test/support/fixtures/cloud/cy-prompt/test-cy-prompt.ts
@@ -2,14 +2,15 @@
 
 import type { CyPromptServerShape, CyPromptServerDefaultShape, CyPromptCDPClient } from '@packages/types'
 import type { Router } from 'express'
+import type { Socket } from 'socket.io'
 
 class CyPromptServer implements CyPromptServerShape {
   initializeRoutes (router: Router): void {
     // This is a test implementation that does nothing
   }
 
-  handleBackendRequest (eventName: string, ...args: any[]): Promise<any> {
-    return Promise.resolve()
+  addSocketListeners (socket: Socket): void {
+    // This is a test implementation that does nothing
   }
 
   connectToBrowser (criClient: CyPromptCDPClient): void {
diff --git a/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts b/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
index bbf19ce91af1..a4009743292b 100644
--- a/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
+++ b/packages/server/test/unit/cloud/cy-prompt/CyPromptManager_spec.ts
@@ -57,18 +57,6 @@ describe('lib/cloud/cy-prompt', () => {
     })
   })
 
-  describe('asynchronous method invocation', () => {
-    it('reports an error when a asynchronous method fails', async () => {
-      const error = new Error('foo')
-
-      sinon.stub(cyPrompt, 'handleBackendRequest').throws(error)
-
-      await cyPromptManager.handleBackendRequest('cy:prompt:start', {} as any)
-
-      // TODO: (cy.prompt) test that the error is reported
-    })
-  })
-
   describe('initializeRoutes', () => {
     it('initializes routes', () => {
       sinon.stub(cyPrompt, 'initializeRoutes')
@@ -80,25 +68,14 @@ describe('lib/cloud/cy-prompt', () => {
     })
   })
 
-  describe('handleBackendRequest', () => {
-    it('calls handleBackendRequest on the cy prompt server', () => {
-      sinon.stub(cyPrompt, 'handleBackendRequest')
+  describe('addSocketListeners', () => {
+    it('adds socket listeners', () => {
+      sinon.stub(cyPrompt, 'addSocketListeners')
+      const mockSocket = sinon.stub()
 
-      cyPromptManager.handleBackendRequest('cy:prompt:start', {} as any)
+      cyPromptManager.addSocketListeners(mockSocket)
 
-      expect(cyPrompt.handleBackendRequest).to.be.calledWith('cy:prompt:start', {} as any)
-    })
-
-    it('does not call handleBackendRequest when cy prompt server is not defined', () => {
-      // Set _cyPromptServer to undefined
-      (cyPromptManager as any)._cyPromptServer = undefined
-
-      // Create a spy on invokeSync to verify it's not called
-      const invokeSyncSpy = sinon.spy(cyPromptManager, 'invokeSync')
-
-      cyPromptManager.handleBackendRequest('cy:prompt:start', {} as any)
-
-      expect(invokeSyncSpy).to.not.be.called
+      expect(cyPrompt.addSocketListeners).to.be.calledWith(mockSocket)
     })
   })
 
diff --git a/packages/server/test/unit/socket_spec.js b/packages/server/test/unit/socket_spec.js
index ec2d3878202b..4a1104cf7036 100644
--- a/packages/server/test/unit/socket_spec.js
+++ b/packages/server/test/unit/socket_spec.js
@@ -90,7 +90,7 @@ describe('lib/socket', () => {
 
         // Create a mock cy prompt object with handleBackendRequest method
         const mockCyPrompt = {
-          handleBackendRequest: sinon.stub().resolves({ foo: 'bar' }),
+          addSocketListeners: sinon.stub(),
           status: 'INITIALIZED',
         }
 
@@ -580,30 +580,6 @@ describe('lib/socket', () => {
       })
     })
 
-    context('on(backend:request, cy:prompt)', () => {
-      it('calls handleBackendRequest with the correct arguments', async function () {
-        // Verify that registerCyPromptReadyListener was called
-        expect(ctx.coreData.cyPromptLifecycleManager.registerCyPromptReadyListener).to.be.called
-
-        // Check that the callback was called with the mock cy prompt object
-        const registerCyPromptReadyListenerCallback = ctx.coreData.cyPromptLifecycleManager.registerCyPromptReadyListener.firstCall.args[0]
-
-        // Verify the mock cy prompt's handleBackendRequest was called by the callback
-        const mockCyPrompt = { handleBackendRequest: sinon.stub().resolves({ foo: 'bar' }) }
-
-        await registerCyPromptReadyListenerCallback(mockCyPrompt)
-
-        await new Promise((resolve) => {
-          this.client.emit('backend:request', 'cy:prompt:init', 'foo', (resp) => {
-            expect(resp.response).to.deep.eq({ foo: 'bar' })
-            expect(mockCyPrompt.handleBackendRequest).to.be.calledWith('cy:prompt:init', 'foo')
-
-            resolve()
-          })
-        })
-      })
-    })
-
     context('on(save:app:state)', () => {
       it('calls onSavedStateChanged with the state', function (done) {
         return this.client.emit('save:app:state', { reporterWidth: 500 }, () => {
@@ -687,6 +663,22 @@ describe('lib/socket', () => {
       })
     })
 
+    context('cy.prompt.addSocketListeners', () => {
+      it('calls addSocketListeners on cy prompt when socket connects', function () {
+        // Verify that registerCyPromptReadyListener was called
+        expect(ctx.coreData.cyPromptLifecycleManager.registerCyPromptReadyListener).to.be.called
+
+        const registerCyPromptReadyListenerCallback = ctx.coreData.cyPromptLifecycleManager.registerCyPromptReadyListener.firstCall.args[0]
+
+        expect(registerCyPromptReadyListenerCallback).to.be.a('function')
+
+        const mockCyPrompt = { addSocketListeners: sinon.stub() }
+
+        registerCyPromptReadyListenerCallback(mockCyPrompt)
+        expect(mockCyPrompt.addSocketListeners).to.be.called
+      })
+    })
+
     context('#isRunnerSocketConnected', function () {
       it('returns false when runner is not connected', function () {
         expect(this.socket.isRunnerSocketConnected()).to.eq(false)
diff --git a/packages/types/src/config.ts b/packages/types/src/config.ts
index 84b11e45aed9..0c5018bbb3d5 100644
--- a/packages/types/src/config.ts
+++ b/packages/types/src/config.ts
@@ -30,7 +30,7 @@ export interface FullConfig extends Partial<Cypress.RuntimeConfigOptions & Cypre
 // and are required when creating a project.
 export type ReceivedCypressOptions =
   Pick<Cypress.RuntimeConfigOptions, 'hosts' | 'projectName' | 'clientRoute' | 'devServerPublicPathRoute' | 'namespace' | 'report' | 'socketIoCookie' | 'configFile' | 'isTextTerminal' | 'isNewProject' | 'proxyUrl' | 'browsers' | 'browserUrl' | 'socketIoRoute' | 'arch' | 'platform' | 'spec' | 'specs' | 'browser' | 'version' | 'remote'>
-  & Pick<Cypress.ResolvedConfigOptions, 'chromeWebSecurity' | 'supportFolder' | 'experimentalSourceRewriting' | 'fixturesFolder' | 'reporter' | 'reporterOptions' | 'screenshotsFolder' | 'supportFile' | 'baseUrl' | 'viewportHeight' | 'viewportWidth' | 'port' | 'experimentalInteractiveRunEvents' | 'userAgent' | 'downloadsFolder' | 'env' | 'excludeSpecPattern' | 'specPattern' | 'experimentalModifyObstructiveThirdPartyCode' | 'injectDocumentDomain' | 'video' | 'videoCompression' | 'videosFolder' | 'resolvedNodeVersion' | 'resolvedNodePath' | 'trashAssetsBeforeRuns' | 'experimentalWebKitSupport' | 'justInTimeCompile' | 'experimentalPromptCommand'> // TODO: Figure out how to type this better.
+  & Pick<Cypress.ResolvedConfigOptions, 'chromeWebSecurity' | 'supportFolder' | 'experimentalSourceRewriting' | 'fixturesFolder' | 'reporter' | 'reporterOptions' | 'screenshotsFolder' | 'supportFile' | 'baseUrl' | 'viewportHeight' | 'viewportWidth' | 'port' | 'experimentalInteractiveRunEvents' | 'userAgent' | 'downloadsFolder' | 'env' | 'excludeSpecPattern' | 'specPattern' | 'experimentalModifyObstructiveThirdPartyCode' | 'injectDocumentDomain' | 'video' | 'videoCompression' | 'videosFolder' | 'resolvedNodeVersion' | 'resolvedNodePath' | 'trashAssetsBeforeRuns' | 'experimentalWebKitSupport' | 'justInTimeCompile'> // TODO: Figure out how to type this better.
 
 export interface SettingsOptions {
   testingType?: 'component' |'e2e'
diff --git a/packages/types/src/cy-prompt/cy-prompt-server-types.ts b/packages/types/src/cy-prompt/cy-prompt-server-types.ts
index be0df63c42ad..b212f1910664 100644
--- a/packages/types/src/cy-prompt/cy-prompt-server-types.ts
+++ b/packages/types/src/cy-prompt/cy-prompt-server-types.ts
@@ -1,12 +1,9 @@
-// Note: This file is owned by the cloud delivered
-// cy prompt bundle. It is downloaded and copied here.
-// It should not be modified directly here.
-
 /// <reference types="cypress" />
 
 import type ProtocolMapping from 'devtools-protocol/types/protocol-mapping.d'
 import type { Router } from 'express'
 import type { AxiosInstance } from 'axios'
+import type { Socket } from 'socket.io'
 
 export type CyPromptCommands = ProtocolMapping.Commands
 
@@ -56,7 +53,7 @@ export interface CyPromptCDPClient {
 
 export interface CyPromptServerShape {
   initializeRoutes(router: Router): void
-  handleBackendRequest: (eventName: string, ...args: any[]) => Promise<any>
+  addSocketListeners(socket: Socket): void
   connectToBrowser: (cdpClient: CyPromptCDPClient) => void
 }