diff --git a/src/Microsoft.AspNet.Server.WebListener/MessagePump.cs b/src/Microsoft.AspNet.Server.WebListener/MessagePump.cs
index bcf7ba653f..890f9b9e63 100644
--- a/src/Microsoft.AspNet.Server.WebListener/MessagePump.cs
+++ b/src/Microsoft.AspNet.Server.WebListener/MessagePump.cs
@@ -39,6 +39,10 @@ namespace Microsoft.AspNet.Server.WebListener
         private int _acceptorCounts;
         private Action<object> _processRequest;
 
+        private bool _stopping;
+        private int _outstandingRequests;
+        private ManualResetEvent _shutdownSignal;
+
         // TODO: private IDictionary<string, object> _capabilities;
 
         internal MessagePump(Microsoft.Net.Server.WebListener listener, ILoggerFactory loggerFactory)
@@ -49,6 +53,7 @@ namespace Microsoft.AspNet.Server.WebListener
 
             _processRequest = new Action<object>(ProcessRequestAsync);
             _maxAccepts = DefaultMaxAccepts;
+            _shutdownSignal = new ManualResetEvent(false);
         }
 
         internal Microsoft.Net.Server.WebListener Listener
@@ -108,7 +113,7 @@ namespace Microsoft.AspNet.Server.WebListener
         private async void ProcessRequestsWorker()
         {
             int workerIndex = Interlocked.Increment(ref _acceptorCounts);
-            while (_listener.IsListening && workerIndex <= MaxAccepts)
+            while (!_stopping && workerIndex <= MaxAccepts)
             {
                 // Receive a request
                 RequestContext requestContext;
@@ -124,7 +129,7 @@ namespace Microsoft.AspNet.Server.WebListener
                 }
                 try
                 {
-                    Task.Factory.StartNew(_processRequest, requestContext);
+                    Task ignored = Task.Factory.StartNew(_processRequest, requestContext);
                 }
                 catch (Exception ex)
                 {
@@ -141,11 +146,18 @@ namespace Microsoft.AspNet.Server.WebListener
             var requestContext = requestContextObj as RequestContext;
             try
             {
+                if (_stopping)
+                {
+                    SetFatalResponse(requestContext, 503);
+                    return;
+                }
                 try
                 {
+                    Interlocked.Increment(ref _outstandingRequests);
                     FeatureContext featureContext = new FeatureContext(requestContext);
                     await _appFunc(featureContext.Features).SupressContext();
                     // TODO: WebSocket/Opaque upgrade - await requestContext.ProcessResponseAsync().SupressContext();
+                    requestContext.Dispose();
                 }
                 catch (Exception ex)
                 {
@@ -157,10 +169,16 @@ namespace Microsoft.AspNet.Server.WebListener
                     else
                     {
                         // We haven't sent a response yet, try to send a 500 Internal Server Error
-                        SetFatalResponse(requestContext);
+                        SetFatalResponse(requestContext, 500);
+                    }
+                }
+                finally
+                {
+                    if (Interlocked.Decrement(ref _outstandingRequests) == 0 && _stopping)
+                    {
+                        _shutdownSignal.Set();
                     }
                 }
-                requestContext.Dispose();
             }
             catch (Exception ex)
             {
@@ -169,16 +187,24 @@ namespace Microsoft.AspNet.Server.WebListener
             }
         }
 
-        private static void SetFatalResponse(RequestContext context)
+        private static void SetFatalResponse(RequestContext context, int status)
         {
-            context.Response.StatusCode = 500;
+            context.Response.StatusCode = status;
             context.Response.ReasonPhrase = string.Empty;
             context.Response.Headers.Clear();
             context.Response.ContentLength = 0;
+            context.Dispose();
         }
 
         public void Dispose()
         {
+            _stopping = true;
+            // Wait for active requests to drain
+            if (_outstandingRequests > 0)
+            {
+                _shutdownSignal.WaitOne();
+            }
+            // All requests are finished
             _listener.Dispose();
         }
     }
diff --git a/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ServerTests.cs b/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ServerTests.cs
index c6f47bb48c..0b84f3a63a 100644
--- a/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ServerTests.cs
+++ b/test/Microsoft.AspNet.Server.WebListener.FunctionalTests/ServerTests.cs
@@ -80,6 +80,26 @@ namespace Microsoft.AspNet.Server.WebListener
             }
         }
 
+        [Fact]
+        public async Task Server_ShutdownDurringRequest_Success()
+        {
+            Task<string> responseTask;
+            ManualResetEvent received = new ManualResetEvent(false);
+            using (Utilities.CreateHttpServer(env =>
+                {
+                    received.Set();
+                    var httpContext = new DefaultHttpContext((IFeatureCollection)env);
+                    httpContext.Response.ContentLength = 11;
+                    return httpContext.Response.WriteAsync("Hello World");
+                }))
+            {
+                responseTask = SendRequestAsync(Address);
+                Assert.True(received.WaitOne(10000));
+            }
+            string response = await responseTask;
+            Assert.Equal("Hello World", response);
+        }
+
         [Fact]
         public void Server_AppException_ClientReset()
         {