diff --git a/src/agent/runtime/index.ts b/src/agent/runtime/index.ts
index 56b1551cc5..af85a7320e 100644
--- a/src/agent/runtime/index.ts
+++ b/src/agent/runtime/index.ts
@@ -849,6 +849,14 @@ export class AgentRuntime {
     };
     const chain = new MiddlewareChain(this.config.middleware);
 
+    // Hold the in-flight agent-loop promise so stream cancellation can detach a
+    // no-op rejection handler. When the client cancels, we abort the shared
+    // signal; the loop (model fetch / tool execution) then rejects with an
+    // AbortError. The `start` body awaits it, but cancellation can land after
+    // that await settles, leaving the rejection without a consumer — fatal as
+    // an unhandled rejection under Deno (#2334).
+    let inFlight: Promise<AgentResponse> | undefined;
+
     return new ReadableStream<Uint8Array>({
       start: async (controller) => {
         try {
@@ -870,7 +878,7 @@ export class AgentRuntime {
               model: effectiveModel,
             },
           });
-          const response = await chain.execute(
+          inFlight = chain.execute(
             agentContext,
             () =>
               this.executeAgentLoopStreaming(
@@ -890,6 +898,7 @@ export class AgentRuntime {
                 streamAbortSignal,
               ),
           );
+          const response = await inFlight;
           throwIfAborted(streamAbortSignal);
           callbacks?.onFinish?.(response);
           throwIfAborted(streamAbortSignal);
@@ -914,7 +923,18 @@ export class AgentRuntime {
         }
       },
       cancel(reason) {
-        streamAbortController.abort(reason);
+        // The client disconnected (e.g. the Chat Stop button). Treat this as a
+        // clean stop: detach a no-op handler from the in-flight loop so the
+        // AbortError it throws when we abort the shared signal cannot surface as
+        // an unhandled rejection, then abort. Guard the abort itself so a
+        // synchronous signal-abort rejection can never escape here (#2334).
+        inFlight?.catch(() => {});
+        try {
+          streamAbortController.abort(reason);
+        } catch {
+          // Aborting an already-aborted controller, or a synchronous reject
+          // from a signal consumer, is a no-op for cancellation purposes.
+        }
       },
     });
   }
diff --git a/src/agent/runtime/runtime-stream-cancel.test.ts b/src/agent/runtime/runtime-stream-cancel.test.ts
new file mode 100644
index 0000000000..02e77f2d68
--- /dev/null
+++ b/src/agent/runtime/runtime-stream-cancel.test.ts
@@ -0,0 +1,164 @@
+import "#veryfront/schemas/_test-setup.ts";
+import { assert } from "#veryfront/testing/assert.ts";
+import { describe, it } from "#veryfront/testing/bdd.ts";
+import { type ModelRuntime } from "#veryfront/provider";
+import { tool } from "#veryfront/tool";
+import { defineSchema } from "#veryfront/schemas/index.ts";
+import { agent } from "../index.ts";
+
+/**
+ * Regression coverage for #2334: cancelling an in-flight agent run must be
+ * treated as a clean stop, not surface as an uncaught `AbortError`.
+ *
+ * The reproduction cancels the response body's reader (exactly what Deno's HTTP
+ * server does when the client disconnects / hits the Chat "Stop" button) while
+ * the model stream — and a tool execution — are still in flight. Before the fix
+ * the runtime's stream `cancel` aborted the shared signal with the client's
+ * foreign reason, and the resulting rejection propagated with no handler,
+ * crashing the process under Deno. Deno's test runner fails on any unhandled
+ * rejection, so these tests fail loudly if the regression returns.
+ */
+
+function flushMicrotasks(): Promise<void> {
+  return new Promise((resolve) => setTimeout(resolve, 20));
+}
+
+/** A model stream that stays open until the run is aborted, then rejects its
+ * pending read with the abort reason — mirroring a real provider fetch body. */
+function createPendingModelStream(abortSignal: AbortSignal | undefined): ReadableStream<unknown> {
+  return new ReadableStream<unknown>({
+    start(controller) {
+      controller.enqueue({ type: "text-start", id: "t" });
+      controller.enqueue({ type: "text-delta", id: "t", delta: "thinking" });
+
+      if (!abortSignal) {
+        return;
+      }
+      if (abortSignal.aborted) {
+        controller.error(abortSignal.reason);
+        return;
+      }
+      abortSignal.addEventListener("abort", () => {
+        controller.error(abortSignal.reason);
+      }, { once: true });
+    },
+  });
+}
+
+describe("agent runtime stream cancellation (#2334)", () => {
+  it("cancelling a model-streaming run does not raise an unhandled AbortError", async () => {
+    const model: ModelRuntime = {
+      provider: "hosted",
+      modelId: "hosted/cancel-crash-model",
+      async doGenerate() {
+        return {
+          content: [],
+          finishReason: "stop",
+          usage: { inputTokens: 0, outputTokens: 0, totalTokens: 0 },
+        };
+      },
+      async doStream(options: unknown) {
+        const abortSignal = (options as { abortSignal?: AbortSignal }).abortSignal;
+        return { stream: createPendingModelStream(abortSignal) };
+      },
+    };
+
+    const assistant = agent({
+      model: "hosted/cancel-crash-model",
+      system: "cancel crash test",
+      maxSteps: 1,
+      resolveModelTransport: async () => ({ model }),
+    });
+
+    const response = (await assistant.stream({ input: "hi" })).toDataStreamResponse();
+    const body = response.body;
+    assert(body !== null, "expected a streaming response body");
+
+    const reader = body.getReader();
+    // Pull the opening frames so the run is genuinely mid-stream.
+    await reader.read();
+    // The client disconnects: cancel with a foreign AbortError reason, exactly
+    // as Deno hands to the stream's cancel algorithm.
+    await reader.cancel(new DOMException("client disconnected", "AbortError"));
+
+    await flushMicrotasks();
+    assert(true, "cancellation completed without an unhandled rejection");
+  });
+
+  it("cancelling while a tool is executing does not raise an unhandled AbortError", async () => {
+    let releaseTool: (() => void) | undefined;
+    const toolStarted = Promise.withResolvers<void>();
+
+    const slowTool = tool({
+      id: "slow_tool",
+      description: "A tool that stays in flight until the run is cancelled",
+      inputSchema: defineSchema((v) => v.object({}))(),
+      execute: async (_input, context) => {
+        toolStarted.resolve();
+        const abortSignal = (context as { abortSignal?: AbortSignal })?.abortSignal;
+        await new Promise<void>((resolve) => {
+          releaseTool = resolve;
+          abortSignal?.addEventListener("abort", () => resolve(), { once: true });
+        });
+        return { ok: true };
+      },
+    });
+
+    let call = 0;
+    const model: ModelRuntime = {
+      provider: "hosted",
+      modelId: "hosted/cancel-crash-tool",
+      async doGenerate() {
+        return {
+          content: [],
+          finishReason: "stop",
+          usage: { inputTokens: 0, outputTokens: 0, totalTokens: 0 },
+        };
+      },
+      async doStream(options: unknown) {
+        call += 1;
+        const abortSignal = (options as { abortSignal?: AbortSignal }).abortSignal;
+        if (call === 1) {
+          // First step: emit a tool call so a tool execution opens.
+          return {
+            stream: new ReadableStream<unknown>({
+              start(controller) {
+                controller.enqueue({
+                  type: "tool-call",
+                  toolCallId: "slow-1",
+                  toolName: "slow_tool",
+                  input: "{}",
+                });
+                controller.enqueue({ type: "finish", finishReason: "tool-calls" });
+                controller.close();
+              },
+            }),
+          };
+        }
+        // Any later step stays open until aborted.
+        return { stream: createPendingModelStream(abortSignal) };
+      },
+    };
+
+    const assistant = agent({
+      model: "hosted/cancel-crash-tool",
+      system: "cancel crash tool test",
+      tools: { slow_tool: slowTool },
+      maxSteps: 3,
+      resolveModelTransport: async () => ({ model }),
+    });
+
+    const response = (await assistant.stream({ input: "run the tool" })).toDataStreamResponse();
+    const body = response.body;
+    assert(body !== null, "expected a streaming response body");
+
+    const reader = body.getReader();
+    await reader.read();
+    await toolStarted.promise;
+    await reader.cancel(new DOMException("client disconnected", "AbortError"));
+    releaseTool?.();
+
+    await flushMicrotasks();
+    assert(true, "cancellation during tool execution completed cleanly");
+  });
+});
diff --git a/src/agent/streaming/tool-execution-data-event-bridge.test.ts b/src/agent/streaming/tool-execution-data-event-bridge.test.ts
index 1173e433b6..a4bfda26fc 100644
--- a/src/agent/streaming/tool-execution-data-event-bridge.test.ts
+++ b/src/agent/streaming/tool-execution-data-event-bridge.test.ts
@@ -93,4 +93,51 @@ describe("createToolExecutionDataEventBridgeStream", () => {
     controller.close();
     await reader.cancel();
   });
+
+  it("cancel resolves cleanly when the base reader cancel rejects (#2334)", async () => {
+    // Mirrors the production crash: the upstream agent runtime's stream cancel
+    // aborts an in-flight signal, and the rejection propagates back through the
+    // base reader's cancel. The bridge must absorb it so cancellation does not
+    // escape as an unhandled rejection (fatal under Deno).
+    const stream = createToolExecutionDataEventBridgeStream({
+      baseStream: new ReadableStream<Uint8Array>({
+        start(controller) {
+          controller.enqueue(new TextEncoder().encode('data: {"type":"message-start"}\n\n'));
+        },
+        cancel() {
+          throw new DOMException("The signal has been aborted", "AbortError");
+        },
+      }),
+      installPublisher() {},
+    });
+
+    const reader = stream.getReader();
+    await reader.read();
+
+    // Must not reject — before the fix this surfaced the base reader's
+    // AbortError to the (often un-awaiting) consumer.
+    await reader.cancel(new DOMException("client disconnected", "AbortError"));
+  });
+
+  it("cancel still forwards the reason to the base reader on the happy path", async () => {
+    let cancelledWith: unknown = "unset";
+    const stream = createToolExecutionDataEventBridgeStream({
+      baseStream: new ReadableStream<Uint8Array>({
+        start(controller) {
+          controller.enqueue(new TextEncoder().encode('data: {"type":"message-start"}\n\n'));
+        },
+        cancel(reason) {
+          cancelledWith = reason;
+        },
+      }),
+      installPublisher() {},
+    });
+
+    const reader = stream.getReader();
+    await reader.read();
+    const reason = new DOMException("client disconnected", "AbortError");
+    await reader.cancel(reason);
+
+    assertEquals(cancelledWith, reason);
+  });
 });
diff --git a/src/agent/streaming/tool-execution-data-event-bridge.ts b/src/agent/streaming/tool-execution-data-event-bridge.ts
index 7e6c2dd9d5..39a5455a49 100644
--- a/src/agent/streaming/tool-execution-data-event-bridge.ts
+++ b/src/agent/streaming/tool-execution-data-event-bridge.ts
@@ -83,7 +83,16 @@ export function createToolExecutionDataEventBridgeStream(
       })();
     },
     async cancel(reason) {
-      await baseReader?.cancel(reason);
+      // Cancellation is best-effort teardown (the client disconnected / hit
+      // Stop). Forwarding the cancel to the base reader can reject — e.g. the
+      // upstream agent runtime aborts an in-flight signal whose rejection
+      // surfaces through the cancel chain. Swallow it so it does not escape as
+      // an unhandled rejection, which is fatal under Deno (#2334).
+      try {
+        await baseReader?.cancel(reason);
+      } catch {
+        // Stream is being torn down; a failed cancel is a clean stop here.
+      }
     },
   });
 }