diff --git a/.editorconfig b/.editorconfig
index 6e89449c1..c1f291525 100644
--- a/.editorconfig
+++ b/.editorconfig
@@ -202,7 +202,7 @@ dotnet_code_quality.ca2208.api_surface=public
 dotnet_diagnostic.ca1822.severity=none
 
 # License header
-file_header_template= Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.\r\nSPDX-License-Identifier: Apache-2.0
+file_header_template= Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.\nSPDX-License-Identifier: Apache-2.0
 
 # ReSharper properties
 resharper_braces_for_for=required
diff --git a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Extensions/ResultExtensions.cs b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Extensions/ResultExtensions.cs
new file mode 100644
index 000000000..ab9e416ad
--- /dev/null
+++ b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Extensions/ResultExtensions.cs
@@ -0,0 +1,33 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+
+using Amazon.Lambda.TestTool.Models;
+
+namespace Amazon.Lambda.TestTool.Extensions;
+
+/// <summary>
+/// A class for common API Gateway responses.
+/// </summary>
+public static class ApiGatewayResults
+{
+    /// <summary>
+    /// Returns a 'Not Found' for HTTP API Gateway mode and 'Missing Authentication Token' for Rest.
+    /// </summary>
+    /// <param name="context">The <see cref="HttpContext"/> to update.</param>
+    /// <param name="emulatorMode">The API Gateway Emulator mode.</param>
+    /// <returns></returns>
+    public static IResult RouteNotFound(HttpContext context, ApiGatewayEmulatorMode emulatorMode)
+    {
+        if (emulatorMode == ApiGatewayEmulatorMode.Rest)
+        {
+            context.Response.StatusCode = StatusCodes.Status403Forbidden;
+            context.Response.Headers.Append("x-amzn-errortype", "MissingAuthenticationTokenException");
+            return Results.Json(new { message = "Missing Authentication Token" });
+        }
+        else
+        {
+            context.Response.StatusCode = StatusCodes.Status404NotFound;
+            return Results.Json(new { message = "Not Found" });
+        }
+    }
+}
diff --git a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Models/Exceptions.cs b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Models/Exceptions.cs
index 4ad1b75f2..1e2d31af1 100644
--- a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Models/Exceptions.cs
+++ b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Models/Exceptions.cs
@@ -6,7 +6,15 @@ namespace Amazon.Lambda.TestTool.Models;
 /// <summary>
 /// Represents a base exception that is thrown by the test tool.
 /// </summary>
-/// <param name="message"></param>
-/// <param name="innerException"></param>
+/// <param name="message">The message used in the exception.</param>
+/// <param name="innerException">The inner exception, if any.</param>
 public abstract class TestToolException(string message, Exception? innerException = null)
     : Exception(message, innerException);
+
+/// <summary>
+/// Thrown if the API Gateway Emulator mode was not provided,
+/// </summary>
+/// <param name="message">The message used in the exception.</param>
+/// <param name="innerException">The inner exception, if any.</param>
+public class InvalidApiGatewayModeException(string message, Exception? innerException = null)
+    : TestToolException(message, innerException);
diff --git a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/ApiGatewayEmulatorProcess.cs b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/ApiGatewayEmulatorProcess.cs
index 3fa3eeef8..5a1e1d1a3 100644
--- a/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/ApiGatewayEmulatorProcess.cs
+++ b/Tools/LambdaTestTool-v2/src/Amazon.Lambda.TestTool/Processes/ApiGatewayEmulatorProcess.cs
@@ -33,6 +33,11 @@ public class ApiGatewayEmulatorProcess
     /// </summary>
     public static ApiGatewayEmulatorProcess Startup(RunCommandSettings settings, CancellationToken cancellationToken = default)
     {
+        if (settings.ApiGatewayEmulatorMode is null)
+        {
+            throw new InvalidApiGatewayModeException("The API Gateway emulator mode was not provided.");
+        }
+
         var builder = WebApplication.CreateBuilder();
 
         builder.Services.AddApiGatewayEmulatorServices();
@@ -61,9 +66,7 @@ public static ApiGatewayEmulatorProcess Startup(RunCommandSettings settings, Can
             {
                 app.Logger.LogInformation("Unable to find a configured Lambda route for the specified method and path: {Method} {Path}",
                     context.Request.Method, context.Request.Path);
-                context.Response.StatusCode = StatusCodes.Status403Forbidden;
-                context.Response.Headers.Append("x-amzn-errortype", "MissingAuthenticationTokenException");
-                return Results.Json(new { message = "Missing Authentication Token" });
+                return ApiGatewayResults.RouteNotFound(context, (ApiGatewayEmulatorMode) settings.ApiGatewayEmulatorMode);
             }
 
             if (settings.ApiGatewayEmulatorMode.Equals(ApiGatewayEmulatorMode.HttpV2))
diff --git a/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Helpers/TestHelpers.cs b/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Helpers/TestHelpers.cs
index 578379453..deba2f4fa 100644
--- a/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Helpers/TestHelpers.cs
+++ b/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Helpers/TestHelpers.cs
@@ -31,6 +31,14 @@ internal static async Task<bool> WaitForApiToStartAsync(string url, int maxRetri
         }
     }
 
+    internal static async Task<HttpResponseMessage> SendRequest(string url)
+    {
+        using (var client = new HttpClient())
+        {
+            return await client.GetAsync(url);
+        }
+    }
+
     internal static async Task CancelAndWaitAsync(Task executeTask)
     {
         await Task.Delay(1000);
diff --git a/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Processes/ApiGatewayEmulatorProcessTests.cs b/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Processes/ApiGatewayEmulatorProcessTests.cs
new file mode 100644
index 000000000..55cb7a6ef
--- /dev/null
+++ b/Tools/LambdaTestTool-v2/tests/Amazon.Lambda.TestTool.UnitTests/Processes/ApiGatewayEmulatorProcessTests.cs
@@ -0,0 +1,38 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+
+using System.Net;
+using Amazon.Lambda.TestTool.Commands.Settings;
+using Amazon.Lambda.TestTool.Models;
+using Amazon.Lambda.TestTool.Processes;
+using Amazon.Lambda.TestTool.UnitTests.Helpers;
+
+namespace Amazon.Lambda.TestTool.UnitTests.Processes;
+
+public class ApiGatewayEmulatorProcessTests
+{
+    [Theory]
+    [InlineData(ApiGatewayEmulatorMode.Rest, HttpStatusCode.Forbidden, "{\"message\":\"Missing Authentication Token\"}")]
+    [InlineData(ApiGatewayEmulatorMode.HttpV1, HttpStatusCode.NotFound, "{\"message\":\"Not Found\"}")]
+    [InlineData(ApiGatewayEmulatorMode.HttpV2, HttpStatusCode.NotFound, "{\"message\":\"Not Found\"}")]
+    public async Task RouteNotFound(ApiGatewayEmulatorMode mode, HttpStatusCode statusCode, string body)
+    {
+        // Arrange
+        var cancellationSource = new CancellationTokenSource();
+        cancellationSource.CancelAfter(5000);
+        var settings = new RunCommandSettings { ApiGatewayEmulatorPort = 9003,  ApiGatewayEmulatorMode = mode, NoLaunchWindow = true};
+        var apiUrl = $"http://{settings.Host}:{settings.ApiGatewayEmulatorPort}/__lambda_test_tool_apigateway_health__";
+
+        // Act
+        var process = ApiGatewayEmulatorProcess.Startup(settings, cancellationSource.Token);
+        var isApiRunning = await TestHelpers.WaitForApiToStartAsync(apiUrl);
+        var response = await TestHelpers.SendRequest($"{process.ServiceUrl}/invalid");
+        await cancellationSource.CancelAsync();
+
+        // Assert
+        await process.RunningTask;
+        Assert.True(isApiRunning);
+        Assert.Equal(statusCode, response.StatusCode);
+        Assert.Equal(body, await response.Content.ReadAsStringAsync());
+    }
+}