diff --git a/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerMiddleware.cs b/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerMiddleware.cs
index d954e00a44a2..7be8b56869c2 100644
--- a/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerMiddleware.cs
+++ b/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerMiddleware.cs
@@ -132,7 +132,7 @@ private async Task HandleException(HttpContext context, ExceptionDispatchInfo ed
 
                 await _options.ExceptionHandler(context);
 
-                if (context.Response.StatusCode != StatusCodes.Status404NotFound)
+                if (context.Response.StatusCode != StatusCodes.Status404NotFound || _options.AllowStatusCode404Response)
                 {
                     if (_diagnosticListener.IsEnabled() && _diagnosticListener.IsEnabled("Microsoft.AspNetCore.Diagnostics.HandledException"))
                     {
diff --git a/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerOptions.cs b/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerOptions.cs
index e5971ecd777d..370c6e419d60 100644
--- a/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerOptions.cs
+++ b/src/Middleware/Diagnostics/src/ExceptionHandler/ExceptionHandlerOptions.cs
@@ -22,5 +22,14 @@ public class ExceptionHandlerOptions
         /// explicitly provided, the subsequent middleware pipeline will be used by default.
         /// </summary>
         public RequestDelegate ExceptionHandler { get; set; }
+
+        /// <summary>
+        /// This value controls whether the <see cref="ExceptionHandlerMiddleware" /> should
+        /// consider a response with a 404 status code to be a valid result of executing the
+        /// <see cref="ExceptionHandler"/>. The default value is false and the middleware will
+        /// consider 404 status codes to be an error on the server and will therefore rethrow
+        /// the original exception.
+        /// </summary>
+        public bool AllowStatusCode404Response { get; set; }
     }
 }
diff --git a/src/Middleware/Diagnostics/test/UnitTests/ExceptionHandlerTest.cs b/src/Middleware/Diagnostics/test/UnitTests/ExceptionHandlerTest.cs
index 1b8df0af5344..8c33d4a8a1e3 100644
--- a/src/Middleware/Diagnostics/test/UnitTests/ExceptionHandlerTest.cs
+++ b/src/Middleware/Diagnostics/test/UnitTests/ExceptionHandlerTest.cs
@@ -542,5 +542,59 @@ public async Task ExceptionHandlerNotFound_RethrowsOriginalError()
                 && w.EventId == 4
                 && w.Message == "No exception handler was found, rethrowing original exception.");
         }
+
+        [Fact]
+        public async Task ExceptionHandler_CanReturn404Responses_WhenAllowed()
+        {
+            var sink = new TestSink(TestSink.EnableWithTypeName<ExceptionHandlerMiddleware>);
+            var loggerFactory = new TestLoggerFactory(sink, enabled: true);
+
+            using var host = new HostBuilder()
+                .ConfigureWebHost(webHostBuilder =>
+                {
+                    webHostBuilder
+                    .UseTestServer()
+                    .ConfigureServices(services =>
+                    {
+                        services.AddSingleton<ILoggerFactory>(loggerFactory);
+                        services.Configure<ExceptionHandlerOptions>(options =>
+                        {
+                            options.AllowStatusCode404Response = true;
+                            options.ExceptionHandler = httpContext =>
+                            {
+                                httpContext.Response.StatusCode = StatusCodes.Status404NotFound;
+                                return Task.CompletedTask;
+                            };
+                        });
+                    })
+                    .Configure(app =>
+                    {
+                        app.UseExceptionHandler();
+
+                        app.Map("/throw", (innerAppBuilder) =>
+                        {
+                            innerAppBuilder.Run(httpContext =>
+                            {
+                                throw new InvalidOperationException("Something bad happened.");
+                            });
+                        });
+                    });
+                }).Build();
+
+            await host.StartAsync();
+
+            using (var server = host.GetTestServer())
+            {
+                var client = server.CreateClient();
+                var response = await client.GetAsync("throw");
+                Assert.Equal(HttpStatusCode.NotFound, response.StatusCode);
+                Assert.Equal(string.Empty, await response.Content.ReadAsStringAsync());
+            }
+
+            Assert.DoesNotContain(sink.Writes, w =>
+                w.LogLevel == LogLevel.Warning
+                && w.EventId == 4
+                && w.Message == "No exception handler was found, rethrowing original exception.");
+        }
     }
 }