diff --git a/src/Microsoft.AspNet.Server.Kestrel/Http/Listener.cs b/src/Microsoft.AspNet.Server.Kestrel/Http/Listener.cs
index 98de2b440f..5bc7ebdeaf 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Http/Listener.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Http/Listener.cs
@@ -69,7 +69,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Http
                 try
                 {
                     ListenSocket = new UvTcpHandle();
-                    ListenSocket.Init(Thread.Loop);
+                    ListenSocket.Init(Thread.Loop, Thread.QueueCloseHandle);
                     ListenSocket.Bind(new IPEndPoint(IPAddress.Any, port));
                     ListenSocket.Listen(10, _connectionCallback, this);
                     tcs.SetResult(0);
@@ -85,7 +85,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Http
         private void OnConnection(UvStreamHandle listenSocket, int status)
         {
             var acceptSocket = new UvTcpHandle();
-            acceptSocket.Init(Thread.Loop);
+            acceptSocket.Init(Thread.Loop, Thread.QueueCloseHandle);
             listenSocket.Accept(acceptSocket);
 
             var connection = new Connection(this, acceptSocket);
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Infrastructure/KestrelThread.cs b/src/Microsoft.AspNet.Server.Kestrel/Infrastructure/KestrelThread.cs
index fae471eec5..5ef6f101a7 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Infrastructure/KestrelThread.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Infrastructure/KestrelThread.cs
@@ -4,6 +4,7 @@
 using Microsoft.AspNet.Server.Kestrel.Networking;
 using System;
 using System.Collections.Generic;
+using System.Diagnostics;
 using System.Runtime.ExceptionServices;
 using System.Threading;
 using System.Threading.Tasks;
@@ -21,6 +22,8 @@ namespace Microsoft.AspNet.Server.Kestrel
         UvAsyncHandle _post;
         Queue<Work> _workAdding = new Queue<Work>();
         Queue<Work> _workRunning = new Queue<Work>();
+        Queue<CloseHandle> _closeHandleAdding = new Queue<CloseHandle>();
+        Queue<CloseHandle> _closeHandleRunning = new Queue<CloseHandle>();
         object _workSync = new Object();
         bool _stopImmediate = false;
         private ExceptionDispatchInfo _closeError;
@@ -31,10 +34,13 @@ namespace Microsoft.AspNet.Server.Kestrel
             _loop = new UvLoopHandle();
             _post = new UvAsyncHandle();
             _thread = new Thread(ThreadStart);
+            QueueCloseHandle = PostCloseHandle;
         }
 
         public UvLoopHandle Loop { get { return _loop; } }
 
+        public Action<Action<IntPtr>, IntPtr> QueueCloseHandle { get; internal set; }
+
         public Task StartAsync()
         {
             var tcs = new TaskCompletionSource<int>();
@@ -92,6 +98,15 @@ namespace Microsoft.AspNet.Server.Kestrel
             return tcs.Task;
         }
 
+        private void PostCloseHandle(Action<IntPtr> callback, IntPtr handle)
+        {
+            lock (_workSync)
+            {
+                _closeHandleAdding.Enqueue(new CloseHandle { Callback = callback, Handle = handle });
+            }
+            _post.Send();
+        }
+
         private void ThreadStart(object parameter)
         {
             var tcs = (TaskCompletionSource<int>)parameter;
@@ -119,7 +134,7 @@ namespace Microsoft.AspNet.Server.Kestrel
                 _post.Reference();
                 _post.DangerousClose();
                 _engine.Libuv.walk(
-                    _loop, 
+                    _loop,
                     (ptr, arg) =>
                     {
                         var handle = UvMemory.FromIntPtr<UvHandle>(ptr);
@@ -138,12 +153,19 @@ namespace Microsoft.AspNet.Server.Kestrel
 
         private void OnPost()
         {
-            var queue = _workAdding;
+            DoPostWork();
+            DoPostCloseHandle();
+        }
+
+        private void DoPostWork()
+        {
+            Queue<Work> queue;
             lock (_workSync)
             {
+                queue = _workAdding;
                 _workAdding = _workRunning;
+                _workRunning = queue;
             }
-            _workRunning = queue;
             while (queue.Count != 0)
             {
                 var work = queue.Dequeue();
@@ -156,7 +178,7 @@ namespace Microsoft.AspNet.Server.Kestrel
                             tcs =>
                             {
                                 ((TaskCompletionSource<int>)tcs).SetResult(0);
-                            }, 
+                            },
                             work.Completion);
                     }
                 }
@@ -168,11 +190,33 @@ namespace Microsoft.AspNet.Server.Kestrel
                     }
                     else
                     {
-                        // TODO: unobserved exception?
+                        Trace.WriteLine("KestrelThread.DoPostWork " + ex.ToString());
                     }
                 }
             }
         }
+        private void DoPostCloseHandle()
+        {
+            Queue<CloseHandle> queue;
+            lock (_workSync)
+            {
+                queue = _closeHandleAdding;
+                _closeHandleAdding = _closeHandleRunning;
+                _closeHandleRunning = queue;
+            }            
+            while (queue.Count != 0)
+            {
+                var closeHandle = queue.Dequeue();
+                try
+                {
+                    closeHandle.Callback(closeHandle.Handle);
+                }
+                catch (Exception ex)
+                {
+                    Trace.WriteLine("KestrelThread.DoPostCloseHandle " + ex.ToString());
+                }
+            }
+        }
 
         private struct Work
         {
@@ -180,5 +224,10 @@ namespace Microsoft.AspNet.Server.Kestrel
             public object State;
             public TaskCompletionSource<int> Completion;
         }
+        private struct CloseHandle
+        {
+            public Action<IntPtr> Callback;
+            public IntPtr Handle;
+        }
     }
 }
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/Libuv.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/Libuv.cs
index 18e9478f86..c777af7998 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/Libuv.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/Libuv.cs
@@ -128,6 +128,10 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
             handle.Validate(closed: true);
             _uv_close(handle.InternalGetHandle(), close_cb);
         }
+        public void close(IntPtr handle, uv_close_cb close_cb)
+        {
+            _uv_close(handle, close_cb);
+        }
 
         [UnmanagedFunctionPointer(CallingConvention.Cdecl)]
         public delegate void uv_async_cb(IntPtr handle);
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UcAsyncHandle.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UcAsyncHandle.cs
index 7709ebd50c..31e8f9b054 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UcAsyncHandle.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UcAsyncHandle.cs
@@ -12,7 +12,11 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
 
         public void Init(UvLoopHandle loop, Action callback)
         {
-            CreateHandle(loop, loop.Libuv.handle_size(Libuv.HandleType.ASYNC));
+            CreateMemory(
+                loop.Libuv, 
+                loop.ThreadId, 
+                loop.Libuv.handle_size(Libuv.HandleType.ASYNC));
+
             _callback = callback;
             _uv.async_init(loop, this, _uv_async_cb);
         }
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvHandle.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvHandle.cs
index d08a6910d7..fe12f19330 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvHandle.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvHandle.cs
@@ -2,20 +2,40 @@
 // Licensed under the Apache License, Version 2.0. See License.txt in the project root for license information.
 
 using System;
+using System.Threading;
 
 namespace Microsoft.AspNet.Server.Kestrel.Networking
 {
     public abstract class UvHandle : UvMemory
     {
-        static Libuv.uv_close_cb _close_cb = DestroyHandle;
+        static Libuv.uv_close_cb _destroyMemory = DestroyMemory;
+        Action<Action<IntPtr>, IntPtr> _queueCloseHandle;
+
+        unsafe protected void CreateHandle(
+            Libuv uv,
+            int threadId,
+            int size,
+            Action<Action<IntPtr>, IntPtr> queueCloseHandle)
+        {
+            _queueCloseHandle = queueCloseHandle;
+            CreateMemory(uv, threadId, size);
+        }
 
         protected override bool ReleaseHandle()
         {
             var memory = handle;
             if (memory != IntPtr.Zero)
             {
-                _uv.close(this, _close_cb);
                 handle = IntPtr.Zero;
+
+                if (Thread.CurrentThread.ManagedThreadId == ThreadId)
+                {
+                    _uv.close(memory, _destroyMemory);
+                }
+                else
+                {
+                    _queueCloseHandle(memory2 => _uv.close(memory2, _destroyMemory), memory);
+                }
             }
             return true;
         }
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvLoopHandle.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvLoopHandle.cs
index 9ea5cb3d8a..a13ae2ccce 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvLoopHandle.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvLoopHandle.cs
@@ -2,6 +2,7 @@
 // Licensed under the Apache License, Version 2.0. See License.txt in the project root for license information.
 
 using System;
+using System.Threading;
 
 namespace Microsoft.AspNet.Server.Kestrel.Networking
 {
@@ -9,7 +10,11 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
     {
         public void Init(Libuv uv)
         {
-            CreateHandle(uv, uv.loop_size());
+            CreateMemory(
+                uv, 
+                Thread.CurrentThread.ManagedThreadId,
+                uv.loop_size());
+
             _uv.loop_init(this);
         }
 
@@ -30,7 +35,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
             {
                 _uv.loop_close(this);
                 handle = IntPtr.Zero;
-                DestroyHandle(memory);
+                DestroyMemory(memory);
             }
             return true;
         }
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvMemory.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvMemory.cs
index e43e600ec3..c3b3c6ce28 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvMemory.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvMemory.cs
@@ -14,7 +14,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
     public abstract class UvMemory : SafeHandle
     {
         protected Libuv _uv;
-        int _threadId;
+        private int _threadId;
 
         public UvMemory() : base(IntPtr.Zero, true)
         {
@@ -30,19 +30,36 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
             }
         }
 
-        unsafe protected void CreateHandle(Libuv uv, int size)
+        public int ThreadId
+        {
+            get
+            {
+                return _threadId;
+            }
+            private set
+            {
+                _threadId = value;
+            }
+        }
+
+        unsafe protected void CreateMemory(Libuv uv, int threadId, int size)
         {
             _uv = uv;
-            _threadId = Thread.CurrentThread.ManagedThreadId;
-
+            ThreadId = threadId;
+            
             handle = Marshal.AllocCoTaskMem(size);
             *(IntPtr*)handle = GCHandle.ToIntPtr(GCHandle.Alloc(this, GCHandleType.Weak));
         }
 
-        protected void CreateHandle(UvLoopHandle loop, int size)
+        unsafe protected static void DestroyMemory(IntPtr memory)
         {
-            CreateHandle(loop._uv, size);
-            _threadId = loop._threadId;
+            var gcHandlePtr = *(IntPtr*)memory;
+            if (gcHandlePtr != IntPtr.Zero)
+            {
+                var gcHandle = GCHandle.FromIntPtr(gcHandlePtr);
+                gcHandle.Free();
+            }
+            Marshal.FreeCoTaskMem(memory);
         }
 
         internal IntPtr InternalGetHandle()
@@ -57,16 +74,6 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
             Trace.Assert(_threadId == Thread.CurrentThread.ManagedThreadId, "ThreadId is incorrect");
         }
 
-        unsafe protected static void DestroyHandle(IntPtr memory)
-        {
-            var gcHandlePtr = *(IntPtr*)memory;
-            if (gcHandlePtr != IntPtr.Zero)
-            {
-                GCHandle.FromIntPtr(gcHandlePtr).Free();
-            }
-            Marshal.FreeCoTaskMem(memory);
-        }
-
         unsafe public static THandle FromIntPtr<THandle>(IntPtr handle)
         {
             GCHandle gcHandle = GCHandle.FromIntPtr(*(IntPtr*)handle);
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvShutdownReq.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvShutdownReq.cs
index 2606285aa0..ef280549c8 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvShutdownReq.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvShutdownReq.cs
@@ -17,7 +17,10 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
 
         public void Init(UvLoopHandle loop)
         {
-            CreateHandle(loop, loop.Libuv.req_size(Libuv.RequestType.SHUTDOWN));
+            CreateMemory(
+                loop.Libuv, 
+                loop.ThreadId,
+                loop.Libuv.req_size(Libuv.RequestType.SHUTDOWN));
         }
 
         public void Shutdown(UvStreamHandle handle, Action<UvShutdownReq, int, object> callback, object state)
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvTcpHandle.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvTcpHandle.cs
index 96d5ddbbc9..e3f90ad846 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvTcpHandle.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvTcpHandle.cs
@@ -10,7 +10,21 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
     {
         public void Init(UvLoopHandle loop)
         {
-            CreateHandle(loop, loop.Libuv.handle_size(Libuv.HandleType.TCP));
+            CreateMemory(
+                loop.Libuv,
+                loop.ThreadId, 
+                loop.Libuv.handle_size(Libuv.HandleType.TCP));
+
+            _uv.tcp_init(loop, this);
+        }
+
+        public void Init(UvLoopHandle loop, Action<Action<IntPtr>, IntPtr> queueCloseHandle)
+        {
+            CreateHandle(
+                loop.Libuv, 
+                loop.ThreadId,
+                loop.Libuv.handle_size(Libuv.HandleType.TCP), queueCloseHandle);
+
             _uv.tcp_init(loop, this);
         }
 
diff --git a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvWriteRequest.cs b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvWriteRequest.cs
index dee7b6bb66..60228c4eca 100644
--- a/src/Microsoft.AspNet.Server.Kestrel/Networking/UvWriteRequest.cs
+++ b/src/Microsoft.AspNet.Server.Kestrel/Networking/UvWriteRequest.cs
@@ -27,7 +27,10 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
         {
             var requestSize = loop.Libuv.req_size(Libuv.RequestType.WRITE);
             var bufferSize = Marshal.SizeOf(typeof(Libuv.uv_buf_t)) * BUFFER_COUNT;
-            CreateHandle(loop, requestSize + bufferSize);
+            CreateMemory(
+                loop.Libuv,
+                loop.ThreadId,
+                requestSize + bufferSize);
             _bufs = handle + requestSize;
         }
 
@@ -37,17 +40,23 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
             Action<UvWriteReq, int, Exception, object> callback,
             object state)
         {
+            // add GCHandle to keeps this SafeHandle alive while request processing
+            _pins.Add(GCHandle.Alloc(this, GCHandleType.Normal));
+
             var pBuffers = (Libuv.uv_buf_t*)_bufs;
             var nBuffers = bufs.Count;
             if (nBuffers > BUFFER_COUNT)
             {
+                // create and pin buffer array when it's larger than the pre-allocated one
                 var bufArray = new Libuv.uv_buf_t[nBuffers];
                 var gcHandle = GCHandle.Alloc(bufArray, GCHandleType.Pinned);
                 _pins.Add(gcHandle);
                 pBuffers = (Libuv.uv_buf_t*)gcHandle.AddrOfPinnedObject();
             }
+
             for (var index = 0; index != nBuffers; ++index)
             {
+                // create and pin each segment being written
                 var buf = bufs.Array[bufs.Offset + index];
 
                 var gcHandle = GCHandle.Alloc(buf.Array, GCHandleType.Pinned);
@@ -56,6 +65,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
                     gcHandle.AddrOfPinnedObject() + buf.Offset,
                     buf.Count);
             }
+
             _callback = callback;
             _state = state;
             _uv.write(this, handle, pBuffers, nBuffers, _uv_write_cb);
@@ -97,7 +107,7 @@ namespace Microsoft.AspNet.Server.Kestrel.Networking
     {
         protected override bool ReleaseHandle()
         {
-            DestroyHandle(handle);
+            DestroyMemory(handle);
             handle = IntPtr.Zero;
             return true;
         }