diff --git a/src/libraries/System.Net.HttpListener/src/System/Net/Windows/WebSockets/WebSocketBase.cs b/src/libraries/System.Net.HttpListener/src/System/Net/Windows/WebSockets/WebSocketBase.cs
index 982a4766538dfb..a574b3890bf844 100644
--- a/src/libraries/System.Net.HttpListener/src/System/Net/Windows/WebSockets/WebSocketBase.cs
+++ b/src/libraries/System.Net.HttpListener/src/System/Net/Windows/WebSockets/WebSocketBase.cs
@@ -636,6 +636,13 @@ private async Task CloseAsyncCore(WebSocketCloseStatus closeStatus,
                     {
                         _closeReceivedTaskCompletionSource ??= new TaskCompletionSource();
 
+                        // _thisLock MUST be released before starting the CloseOutput operation: it acquires the
+                        // SessionHandle-lock, which MUST always be acquired before _thisLock (see TakeLocks).
+                        // Acquiring the locks in the opposite order here would deadlock with a thread that is
+                        // processing a received close frame, as that one holds the SessionHandle-lock while
+                        // acquiring _thisLock in StartOnCloseReceived.
+                        ReleaseLock(_thisLock, ref lockTaken);
+
                         closeOutputTask = CloseOutputAsync(closeStatus,
                             statusDescription,
                             linkedCancellationToken);
@@ -716,9 +723,13 @@ private async Task CloseAsyncCore(WebSocketCloseStatus closeStatus,
                     ArraySegment<byte> closeMessageBuffer =
                         new ArraySegment<byte>(new byte[HttpWebSocket.MinReceiveBufferSize]);
                     EnsureReceiveOperation();
+
+                    // As above, _thisLock MUST be released before starting the receive operation, because
+                    // WebSocketOperation.Process acquires the SessionHandle-lock.
+                    ReleaseLock(_thisLock, ref lockTaken);
+
                     Task<WebSocketReceiveResult?> receiveAsyncTask = _receiveOperation!.Process(closeMessageBuffer,
                         linkedCancellationToken);
-                    ReleaseLock(_thisLock, ref lockTaken);
 
                     WebSocketReceiveResult? receiveResult = null;
                     try
@@ -816,6 +827,11 @@ private async Task CloseAsyncCore(WebSocketCloseStatus closeStatus,
             catch (Exception exception)
             {
                 bool aborted = linkedCancellationToken.IsCancellationRequested;
+
+                // As above, _thisLock MUST be released before calling Abort, because it acquires the
+                // SessionHandle-lock.
+                ReleaseLock(_thisLock, ref lockTaken);
+
                 Abort();
                 ThrowIfConvertibleException(nameof(CloseAsync), exception, cancellationToken, aborted);
                 throw;
diff --git a/src/libraries/System.Net.HttpListener/tests/HttpListenerWebSocketTests.cs b/src/libraries/System.Net.HttpListener/tests/HttpListenerWebSocketTests.cs
index d1ede4096ba0f8..80106810b4c648 100644
--- a/src/libraries/System.Net.HttpListener/tests/HttpListenerWebSocketTests.cs
+++ b/src/libraries/System.Net.HttpListener/tests/HttpListenerWebSocketTests.cs
@@ -360,6 +360,52 @@ public async Task Abort_CallAfterAborted_Nop()
             Assert.Equal(WebSocketState.Aborted, context.WebSocket.State);
         }
 
+        [ConditionalFact(typeof(Helpers), nameof(Helpers.IsWindowsImplementation))]
+        public async Task CloseAsync_ConcurrentWithCloseFrameFromClient_DoesNotDeadlock()
+        {
+            // Closing a WebSocket from both ends at the same time used to deadlock: the thread processing
+            // an incoming close frame holds the session handle lock while acquiring the state lock, while
+            // CloseAsync held the state lock while acquiring the session handle lock.
+            const int Iterations = 100;
+            Random random = new Random(42);
+
+            for (int i = 0; i < Iterations; i++)
+            {
+                using ClientWebSocket client = new ClientWebSocket();
+                HttpListenerWebSocketContext context = await GetWebSocketContext(client);
+                WebSocket server = context.WebSocket;
+
+                // The pending receive makes a separate thread process the close frame sent by the client.
+                Task serverReceiveTask = IgnoreExpectedExceptionsAsync(
+                    server.ReceiveAsync(new ArraySegment<byte>(new byte[16]), CancellationToken.None));
+
+                Task clientCloseTask = IgnoreExpectedExceptionsAsync(
+                    client.CloseOutputAsync(WebSocketCloseStatus.NormalClosure, null, CancellationToken.None));
+
+                // Sweep the (very short) window in which the deadlock can happen.
+                Thread.SpinWait(random.Next(200_000));
+
+                Task serverCloseTask = IgnoreExpectedExceptionsAsync(Task.Run(
+                    () => server.CloseAsync(WebSocketCloseStatus.NormalClosure, null, CancellationToken.None)));
+
+                Task allTasks = Task.WhenAll(serverReceiveTask, clientCloseTask, serverCloseTask);
+                await allTasks.WaitAsync(TimeSpan.FromSeconds(30));
+
+                server.Dispose();
+            }
+
+            static async Task IgnoreExpectedExceptionsAsync(Task task)
+            {
+                try
+                {
+                    await task;
+                }
+                catch (Exception e) when (e is WebSocketException or InvalidOperationException or ObjectDisposedException or OperationCanceledException)
+                {
+                }
+            }
+        }
+
         [ConditionalFact(typeof(PlatformDetection), nameof(PlatformDetection.IsWindows))]
         public async Task ReceiveAsync_ReadBuffer_WithWindowsAuthScheme_Success()
         {
@@ -430,5 +476,23 @@ private async Task<HttpListenerWebSocketContext> GetWebSocketContext(string[] su
             HttpListenerContext context = await serverContextTask;
             return await context.AcceptWebSocketAsync(null);
         }
+
+        private async Task<HttpListenerWebSocketContext> GetWebSocketContext(ClientWebSocket client)
+        {
+            var uriBuilder = new UriBuilder(Factory.ListeningUrl) { Scheme = "ws" };
+            Task<HttpListenerContext> serverContextTask = Factory.GetListener().GetContextAsync();
+
+            Task clientConnectTask = client.ConnectAsync(uriBuilder.Uri, CancellationToken.None);
+            if (clientConnectTask == await Task.WhenAny(serverContextTask, clientConnectTask))
+            {
+                await clientConnectTask;
+                Assert.Fail("Client should not have completed prior to server sending response");
+            }
+
+            HttpListenerContext context = await serverContextTask;
+            HttpListenerWebSocketContext webSocketContext = await context.AcceptWebSocketAsync(null);
+            await clientConnectTask;
+            return webSocketContext;
+        }
     }
 }