diff --git a/src/ModelContextProtocol.Core/McpSessionHandler.cs b/src/ModelContextProtocol.Core/McpSessionHandler.cs
index b2f94fb28..389a7cf22 100644
--- a/src/ModelContextProtocol.Core/McpSessionHandler.cs
+++ b/src/ModelContextProtocol.Core/McpSessionHandler.cs
@@ -173,12 +173,19 @@ public Task ProcessMessagesAsync(CancellationToken cancellationToken)
 
     private async Task ProcessMessagesCoreAsync(CancellationToken cancellationToken)
     {
+        // Track in-flight message handlers so we can wait for them to complete before returning.
+        // Start at 1 to represent ProcessMessagesCoreAsync itself; it's decremented after the loop exits.
+        int inFlightCount = 1;
+        var allHandlersCompleted = new TaskCompletionSource<bool>(TaskCreationOptions.RunContinuationsAsynchronously);
+
         try
         {
             await foreach (var message in _transport.MessageReader.ReadAllAsync(cancellationToken).ConfigureAwait(false))
             {
                 LogMessageRead(EndpointName, message.GetType().Name);
 
+                Interlocked.Increment(ref inFlightCount);
+
                 // Fire and forget the message handling to avoid blocking the transport.
                 if (message.Context?.ExecutionContext is null)
                 {
@@ -286,6 +293,11 @@ ex is OperationCanceledException &&
                             _handlingRequests.TryRemove(messageWithId.Id, out _);
                             combinedCts!.Dispose();
                         }
+
+                        if (Interlocked.Decrement(ref inFlightCount) == 0)
+                        {
+                            allHandlersCompleted.TrySetResult(true);
+                        }
                     }
                 }
             }
@@ -297,6 +309,12 @@ ex is OperationCanceledException &&
         }
         finally
         {
+            // Decrement our own count. If all handlers have already completed, this will signal completion.
+            if (Interlocked.Decrement(ref inFlightCount) != 0)
+            {
+                await allHandlersCompleted.Task.ConfigureAwait(false);
+            }
+
             // Fail any pending requests, as they'll never be satisfied.
             foreach (var entry in _pendingRequests)
             {
diff --git a/tests/ModelContextProtocol.Tests/Server/McpServerTests.cs b/tests/ModelContextProtocol.Tests/Server/McpServerTests.cs
index ea680ecf0..045cbe435 100644
--- a/tests/ModelContextProtocol.Tests/Server/McpServerTests.cs
+++ b/tests/ModelContextProtocol.Tests/Server/McpServerTests.cs
@@ -1003,6 +1003,60 @@ await transport.SendClientMessageAsync(new JsonRpcNotification
         await runTask;
     }
 
+    [Fact]
+    public async Task RunAsync_WaitsForInFlightHandlersBeforeReturning()
+    {
+        // Arrange: Create a tool handler that blocks until we release it.
+        var handlerStarted = new TaskCompletionSource<bool>(TaskCreationOptions.RunContinuationsAsynchronously);
+        var releaseHandler = new TaskCompletionSource<bool>(TaskCreationOptions.RunContinuationsAsynchronously);
+        bool handlerCompleted = false;
+
+        await using var transport = new TestServerTransport();
+        var options = CreateOptions(new ServerCapabilities { Tools = new() });
+        options.Handlers.CallToolHandler = async (request, ct) =>
+        {
+            handlerStarted.SetResult(true);
+            await releaseHandler.Task;
+            handlerCompleted = true;
+            return new CallToolResult { Content = [new TextContentBlock { Text = "done" }] };
+        };
+        options.Handlers.ListToolsHandler = (request, ct) => throw new NotImplementedException();
+
+        await using var server = McpServer.Create(transport, options, LoggerFactory);
+        var runTask = server.RunAsync(TestContext.Current.CancellationToken);
+
+        // Send a tool call request.
+        await transport.SendClientMessageAsync(
+            new JsonRpcRequest
+            {
+                Method = RequestMethods.ToolsCall,
+                Id = new RequestId(1)
+            },
+            TestContext.Current.CancellationToken);
+
+        // Wait for the handler to start executing.
+        await handlerStarted.Task.WaitAsync(TestConstants.DefaultTimeout, TestContext.Current.CancellationToken);
+
+        // Dispose the transport to simulate client disconnect while the handler is still running.
+        await transport.DisposeAsync();
+
+        // Release the handler after a delay, giving ProcessMessagesCoreAsync time to notice the
+        // channel closed. Without the fix, RunAsync would return before the handler completes.
+        var ct = TestContext.Current.CancellationToken;
+        _ = Task.Run(async () =>
+        {
+            await Task.Delay(200, ct);
+            releaseHandler.SetResult(true);
+        }, ct);
+
+        // Wait for RunAsync to complete.
+        await runTask.WaitAsync(TestConstants.DefaultTimeout, TestContext.Current.CancellationToken);
+
+        // With the fix, RunAsync waits for in-flight handlers. Without it, it returns immediately
+        // after the transport closes (before the 500ms delay releases the handler).
+        Assert.True(handlerCompleted, "RunAsync should wait for in-flight handlers to complete before returning.");
+    }
+
     private static async Task InitializeServerAsync(TestServerTransport transport, ClientCapabilities capabilities, CancellationToken cancellationToken = default)
     {
         var initializeRequest = new JsonRpcRequest