diff --git a/src/Components/Server/src/Builder/ServerRazorComponentsEndpointConventionBuilderExtensions.cs b/src/Components/Server/src/Builder/ServerRazorComponentsEndpointConventionBuilderExtensions.cs
index 0d4a07fefef5..f317213cba0e 100644
--- a/src/Components/Server/src/Builder/ServerRazorComponentsEndpointConventionBuilderExtensions.cs
+++ b/src/Components/Server/src/Builder/ServerRazorComponentsEndpointConventionBuilderExtensions.cs
@@ -6,6 +6,7 @@
 using Microsoft.AspNetCore.Components.Server;
 using Microsoft.AspNetCore.Components.Web;
 using Microsoft.AspNetCore.SignalR;
+using Microsoft.Extensions.Primitives;
 
 namespace Microsoft.AspNetCore.Builder;
 
@@ -54,7 +55,8 @@ public static RazorComponentsEndpointConventionBuilder AddInteractiveServerRende
                         var original = b.RequestDelegate;
                         b.RequestDelegate = async context =>
                         {
-                            context.Response.Headers.Add("Content-Security-Policy", $"frame-ancestors {options.ContentSecurityFrameAncestorsPolicy}");
+                            var headers = context.Response.Headers;
+                            headers.ContentSecurityPolicy = StringValues.Concat(headers.ContentSecurityPolicy, $"frame-ancestors {options.ContentSecurityFrameAncestorsPolicy}");
                             await original(context);
                         };
                     }
diff --git a/src/Components/test/E2ETest/ServerExecutionTests/WebSocketCompressionTests.cs b/src/Components/test/E2ETest/ServerExecutionTests/WebSocketCompressionTests.cs
index a8d1b883c3eb..25812209add8 100644
--- a/src/Components/test/E2ETest/ServerExecutionTests/WebSocketCompressionTests.cs
+++ b/src/Components/test/E2ETest/ServerExecutionTests/WebSocketCompressionTests.cs
@@ -50,6 +50,43 @@ public async Task EmbeddingServerAppInsideIframe_WorksAsync()
             Assert.DoesNotContain("Content-Security-Policy", response.Headers.Select(h => h.Key));
         }
     }
+
+    [Fact]
+    public async Task EmbeddingServerAppInsideIframe_WorksWithMultipleCspHeaders()
+    {
+        Navigate("/subdir/iframe?add-csp");
+
+        var logs = Browser.GetBrowserLogs(LogLevel.Severe);
+
+        Assert.Empty(logs);
+
+        // Get the iframe element from the page, and inspect its contents for a p element with id inside-iframe
+        var iframe = Browser.FindElement(By.TagName("iframe"));
+        Browser.SwitchTo().Frame(iframe);
+        Browser.Exists(By.Id("inside-iframe"));
+
+        using var client = new HttpClient() { BaseAddress = _serverFixture.RootUri };
+        var response = await client.GetAsync("/subdir/iframe?add-csp");
+        response.EnsureSuccessStatusCode();
+
+        if (ExpectedPolicy != null)
+        {
+            Assert.Equal(
+                [
+                    "script-src 'self' 'unsafe-inline'",
+                    $"frame-ancestors {ExpectedPolicy}"
+                ],
+                response.Headers.GetValues("Content-Security-Policy"));
+        }
+        else
+        {
+            Assert.Equal(
+                [
+                    "script-src 'self' 'unsafe-inline'"
+                ],
+                response.Headers.GetValues("Content-Security-Policy"));
+        }
+    }
 }
 
 public abstract partial class BlockedWebSocketCompressionTests(
diff --git a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
index 6dd3c4cb16b6..43c5947926af 100644
--- a/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
+++ b/src/Components/test/testassets/Components.TestServer/RazorComponentEndpointsStartup.cs
@@ -68,6 +68,16 @@ public void Configure(IApplicationBuilder app, IWebHostEnvironment env)
             app.UseRouting();
             UseFakeAuthState(app);
             app.UseAntiforgery();
+
+            app.Use((ctx, nxt) =>
+            {
+                if (ctx.Request.Query.ContainsKey("add-csp"))
+                {
+                    ctx.Response.Headers.Add("Content-Security-Policy", "script-src 'self' 'unsafe-inline'");
+                }
+                return nxt();
+            });
+
             _ = app.UseEndpoints(endpoints =>
             {
                 _ = endpoints.MapRazorComponents<TRootComponent>()