diff --git a/.changeset/abort-handlers-on-close.md b/.changeset/abort-handlers-on-close.md
new file mode 100644
index 000000000..b6bc65e65
--- /dev/null
+++ b/.changeset/abort-handlers-on-close.md
@@ -0,0 +1,5 @@
+---
+'@modelcontextprotocol/core': patch
+---
+
+Abort in-flight request handlers when the connection closes. Previously, request handlers would continue running after the transport disconnected, wasting resources and preventing proper cleanup. Also fixes `InMemoryTransport.close()` firing `onclose` twice on the initiating side.
diff --git a/packages/core/src/shared/protocol.ts b/packages/core/src/shared/protocol.ts
index d82d67da3..836ec3a19 100644
--- a/packages/core/src/shared/protocol.ts
+++ b/packages/core/src/shared/protocol.ts
@@ -494,13 +494,28 @@ export abstract class Protocol<ContextT extends BaseContext> {
         this._taskManager.onClose();
         this._pendingDebouncedNotifications.clear();
 
+        for (const info of this._timeoutInfo.values()) {
+            clearTimeout(info.timeoutId);
+        }
+        this._timeoutInfo.clear();
+
+        const requestHandlerAbortControllers = this._requestHandlerAbortControllers;
+        this._requestHandlerAbortControllers = new Map();
+
         const error = new SdkError(SdkErrorCode.ConnectionClosed, 'Connection closed');
 
         this._transport = undefined;
-        this.onclose?.();
 
-        for (const handler of responseHandlers.values()) {
-            handler(error);
+        try {
+            this.onclose?.();
+        } finally {
+            for (const handler of responseHandlers.values()) {
+                handler(error);
+            }
+
+            for (const controller of requestHandlerAbortControllers.values()) {
+                controller.abort(error);
+            }
         }
     }
 
diff --git a/packages/core/src/shared/taskManager.ts b/packages/core/src/shared/taskManager.ts
index 28460d1d9..2d6f4eeaa 100644
--- a/packages/core/src/shared/taskManager.ts
+++ b/packages/core/src/shared/taskManager.ts
@@ -801,6 +801,7 @@ export class TaskManager {
 
     onClose(): void {
         this._taskProgressTokens.clear();
+        this._requestResolvers.clear();
     }
 
     // -- Private helpers --
diff --git a/packages/core/src/util/inMemory.ts b/packages/core/src/util/inMemory.ts
index 1103b5733..256363c13 100644
--- a/packages/core/src/util/inMemory.ts
+++ b/packages/core/src/util/inMemory.ts
@@ -13,6 +13,7 @@ interface QueuedMessage {
 export class InMemoryTransport implements Transport {
     private _otherTransport?: InMemoryTransport;
     private _messageQueue: QueuedMessage[] = [];
+    private _closed = false;
 
     onclose?: () => void;
     onerror?: (error: Error) => void;
@@ -39,10 +40,16 @@ export class InMemoryTransport implements Transport {
     }
 
     async close(): Promise<void> {
+        if (this._closed) return;
+        this._closed = true;
+
         const other = this._otherTransport;
         this._otherTransport = undefined;
-        await other?.close();
-        this.onclose?.();
+        try {
+            await other?.close();
+        } finally {
+            this.onclose?.();
+        }
     }
 
     /**
diff --git a/packages/core/test/inMemory.test.ts b/packages/core/test/inMemory.test.ts
index 280efdf4b..46332eaa2 100644
--- a/packages/core/test/inMemory.test.ts
+++ b/packages/core/test/inMemory.test.ts
@@ -99,6 +99,53 @@ describe('InMemoryTransport', () => {
         await expect(clientTransport.send({ jsonrpc: '2.0', method: 'test', id: 1 })).rejects.toThrow('Not connected');
     });
 
+    test('should fire onclose exactly once per transport', async () => {
+        let clientCloseCount = 0;
+        let serverCloseCount = 0;
+
+        clientTransport.onclose = () => clientCloseCount++;
+        serverTransport.onclose = () => serverCloseCount++;
+
+        await clientTransport.close();
+
+        expect(clientCloseCount).toBe(1);
+        expect(serverCloseCount).toBe(1);
+    });
+
+    test('should handle double close idempotently', async () => {
+        let clientCloseCount = 0;
+        clientTransport.onclose = () => clientCloseCount++;
+
+        await clientTransport.close();
+        await clientTransport.close();
+
+        expect(clientCloseCount).toBe(1);
+    });
+
+    test('should handle concurrent close from both sides', async () => {
+        let clientCloseCount = 0;
+        let serverCloseCount = 0;
+
+        clientTransport.onclose = () => clientCloseCount++;
+        serverTransport.onclose = () => serverCloseCount++;
+
+        await Promise.all([clientTransport.close(), serverTransport.close()]);
+
+        expect(clientCloseCount).toBe(1);
+        expect(serverCloseCount).toBe(1);
+    });
+
+    test('should fire onclose even if peer onclose throws', async () => {
+        let clientCloseCount = 0;
+        clientTransport.onclose = () => clientCloseCount++;
+        serverTransport.onclose = () => {
+            throw new Error('boom');
+        };
+
+        await expect(clientTransport.close()).rejects.toThrow('boom');
+        expect(clientCloseCount).toBe(1);
+    });
+
     test('should queue messages sent before start', async () => {
         const message: JSONRPCMessage = {
             jsonrpc: '2.0',
diff --git a/packages/core/test/shared/protocol.test.ts b/packages/core/test/shared/protocol.test.ts
index 60e4e6d24..69735bc3a 100644
--- a/packages/core/test/shared/protocol.test.ts
+++ b/packages/core/test/shared/protocol.test.ts
@@ -217,6 +217,36 @@ describe('protocol tests', () => {
         expect(oncloseMock).toHaveBeenCalled();
     });
 
+    test('should abort in-flight request handlers when the connection is closed', async () => {
+        await protocol.connect(transport);
+
+        let abortReason: unknown;
+        let handlerStarted = false;
+        const handlerDone = new Promise<void>(resolve => {
+            protocol.setRequestHandler('ping', async (_request, ctx) => {
+                handlerStarted = true;
+                await new Promise<void>(resolveInner => {
+                    ctx.mcpReq.signal.addEventListener('abort', () => {
+                        abortReason = ctx.mcpReq.signal.reason;
+                        resolveInner();
+                    });
+                });
+                resolve();
+                return {};
+            });
+        });
+
+        transport.onmessage?.({ jsonrpc: '2.0', id: 1, method: 'ping', params: {} });
+
+        await vi.waitFor(() => expect(handlerStarted).toBe(true));
+
+        await transport.close();
+        await handlerDone;
+
+        expect(abortReason).toBeInstanceOf(SdkError);
+        expect((abortReason as SdkError).code).toBe(SdkErrorCode.ConnectionClosed);
+    });
+
     test('should not overwrite existing hooks when connecting transports', async () => {
         const oncloseMock = vi.fn();
         const onerrorMock = vi.fn();