diff --git a/src/libraries/System.Net.HttpListener/src/System/Net/Managed/WebSockets/HttpWebSocket.Managed.cs b/src/libraries/System.Net.HttpListener/src/System/Net/Managed/WebSockets/HttpWebSocket.Managed.cs
index 7c925cb4e315a6..aa83f0eb3f8803 100644
--- a/src/libraries/System.Net.HttpListener/src/System/Net/Managed/WebSockets/HttpWebSocket.Managed.cs
+++ b/src/libraries/System.Net.HttpListener/src/System/Net/Managed/WebSockets/HttpWebSocket.Managed.cs
@@ -1,6 +1,7 @@
 // Licensed to the .NET Foundation under one or more agreements.
 // The .NET Foundation licenses this file to you under the MIT license.
 
+using System.Threading;
 using System.Threading.Tasks;
 
 namespace System.Net.WebSockets
@@ -56,7 +57,12 @@ internal static async Task<HttpListenerWebSocketContext> AcceptWebSocketAsyncCor
             // Send websocket handshake headers
             await responseStream.WriteWebSocketHandshakeHeadersAsync().ConfigureAwait(false);
 
-            WebSocket webSocket = WebSocket.CreateFromStream(context.Connection.ConnectedStream, isServer: true, subProtocol, keepAliveInterval);
+            WebSocket rawWebSocket = WebSocket.CreateFromStream(context.Connection.ConnectedStream, isServer: true, subProtocol, keepAliveInterval);
+
+            // Wrap the raw websocket so its Dispose() automatically closes the connection.
+            // This is important as common and recommended usage is to just Dispose the HttpListenerWebSocketContext.WebSocket
+            // and without it connection would not be cleaned up causing memory leaks and other issues.
+            HttpListenerWrappedWebSocket webSocket = new(rawWebSocket, context);
 
             HttpListenerWebSocketContext webSocketContext = new HttpListenerWebSocketContext(
                                                                 request.Url!,
@@ -76,5 +82,98 @@ internal static async Task<HttpListenerWebSocketContext> AcceptWebSocketAsyncCor
         }
 
         private const bool WebSocketsSupported = true;
+
+        /// <summary>
+        /// Wraps the real WebSocket so that when Dispose() is called,
+        /// we also call context.Response.Close(), triggering UnregisterContext.
+        /// </summary>
+        private sealed class HttpListenerWrappedWebSocket : WebSocket
+        {
+            private readonly WebSocket _inner;
+            private readonly HttpListenerContext _context;
+            private bool _disposed;
+
+            internal HttpListenerWrappedWebSocket(WebSocket inner, HttpListenerContext context)
+            {
+                _inner = inner;
+                _context = context;
+            }
+
+            public override WebSocketCloseStatus? CloseStatus => _inner.CloseStatus;
+            public override string? CloseStatusDescription => _inner.CloseStatusDescription;
+            public override WebSocketState State => _inner.State;
+            public override string? SubProtocol => _inner.SubProtocol;
+
+            public override void Abort() => _inner.Abort();
+
+            public override Task CloseAsync(
+                WebSocketCloseStatus closeStatus,
+                string? statusDescription,
+                CancellationToken cancellationToken) =>
+                _inner.CloseAsync(closeStatus, statusDescription, cancellationToken);
+
+            public override Task CloseOutputAsync(
+                WebSocketCloseStatus closeStatus,
+                string? statusDescription,
+                CancellationToken cancellationToken) =>
+                _inner.CloseOutputAsync(closeStatus, statusDescription, cancellationToken);
+
+            public override void Dispose()
+            {
+                Dispose(true);
+                GC.SuppressFinalize(this);
+            }
+
+            private void Dispose(bool disposing)
+            {
+                if (_disposed)
+                    return;
+                _disposed = true;
+
+                if (disposing)
+                {
+                    // Dispose the underlying raw WebSocket
+                    _inner.Dispose();
+                    // Ensure we remove the context from the HttpListener's tracking dictionary
+                    // by forcibly calling Response.Close(). This closes the underlying connection
+                    // and also calls UnregisterContext(context), preventing stale HttpListenerContext objects causing memory leak.
+                    _context.Response.Close();
+                }
+                else
+                {
+                    // Technically we shouldn't be doing the following work when disposing == false,
+                    // as the following work relies on other finalizable objects.
+                    // But given we have little choice: if someone drops the websocket without
+                    // disposing of it we need to close the context to prevent memory leaks.
+                    try
+                    {
+                        _context.Response.Close();
+                    }
+                    catch
+                    {
+                        // We are doing best effort here to handle the case where the user does not properly Dispose the WebSocket.
+                        // If we fail to close the reponse, we are not going to throw an exception and possibly crash.
+                        // We are just going to ignore it and let the GC do its best.
+                    }
+                }
+            }
+
+            ~HttpListenerWrappedWebSocket()
+            {
+                Dispose(false);
+            }
+
+            public override Task<WebSocketReceiveResult> ReceiveAsync(
+                ArraySegment<byte> buffer,
+                CancellationToken cancellationToken) =>
+                _inner.ReceiveAsync(buffer, cancellationToken);
+
+            public override Task SendAsync(
+                ArraySegment<byte> buffer,
+                WebSocketMessageType messageType,
+                bool endOfMessage,
+                CancellationToken cancellationToken) =>
+                _inner.SendAsync(buffer, messageType, endOfMessage, cancellationToken);
+        }
     }
 }