diff --git a/src/runtime/server/ServerWebSocket.rs b/src/runtime/server/ServerWebSocket.rs
index 5225c12379fb..915ee1894870 100644
--- a/src/runtime/server/ServerWebSocket.rs
+++ b/src/runtime/server/ServerWebSocket.rs
@@ -708,6 +708,13 @@ impl ServerWebSocket {
             return;
         }
 
+        // on_open's error branch closes the socket, landing here with the
+        // termination from its handler still pending. Both branches below
+        // enter JS, which trips assertNoException().
+        if handler.global_object().has_exception() {
+            return;
+        }
+
         // Copy to a stack local before `sig.signal()` re-enters JS: a GC
         // between the test and the `.call(...)` could otherwise collect it.
         let on_close_handler = handler.on_close;
diff --git a/src/runtime/server/WebSocketServerContext.rs b/src/runtime/server/WebSocketServerContext.rs
index 41d8be5ac37d..ce65d055ae8a 100644
--- a/src/runtime/server/WebSocketServerContext.rs
+++ b/src/runtime/server/WebSocketServerContext.rs
@@ -85,6 +85,11 @@ impl Handler {
         global_object: &JSGlobalObject,
         error_value: JSValue,
     ) {
+        // Termination raised inside the preceding callback.call() cannot be
+        // cleared; entering JS again trips executeCallImpl's assertNoException.
+        if global_object.has_exception() {
+            return;
+        }
         if !on_error.is_empty_or_undefined_or_null() {
             let _ = on_error
                 .call(global_object, JSValue::UNDEFINED, &[error_value])
diff --git a/src/runtime/socket/Handlers.rs b/src/runtime/socket/Handlers.rs
index a83944b4153c..8819de1760ed 100644
--- a/src/runtime/socket/Handlers.rs
+++ b/src/runtime/socket/Handlers.rs
@@ -282,6 +282,11 @@ impl Handlers {
         }
 
         let global_object = self.global_object;
+        // Termination raised inside the preceding callback.call() cannot be
+        // cleared; entering JS again trips executeCallImpl's assertNoException.
+        if global_object.has_exception() {
+            return false;
+        }
         let on_error = self.on_error();
 
         if on_error.is_empty() {
diff --git a/src/runtime/socket/socket_body.rs b/src/runtime/socket/socket_body.rs
index f0967f4f7a99..0ed1b63dc8c6 100644
--- a/src/runtime/socket/socket_body.rs
+++ b/src/runtime/socket/socket_body.rs
@@ -2032,6 +2032,14 @@ impl<const SSL: bool> NewSocket<SSL> {
             return Ok(());
         }
 
+        // An earlier callback in this dispatch may have left a termination
+        // pending — on_open's error branch closes the socket from
+        // mark_inactive(), landing here. Entering JS trips assertNoException().
+        if handlers.global_object.has_exception() {
+            drop(cleanup);
+            return Ok(());
+        }
+
         // the handlers must be kept alive for the duration of the function call
         // that way if we need to call the error handler, we can
         let scope = handlers.enter();
diff --git a/test/js/bun/net/socket-handler-worker-terminate.test.ts b/test/js/bun/net/socket-handler-worker-terminate.test.ts
new file mode 100644
index 000000000000..c2d44669de8a
--- /dev/null
+++ b/test/js/bun/net/socket-handler-worker-terminate.test.ts
@@ -0,0 +1,223 @@
+// worker.terminate() firing while a Bun.listen socket handler is mid-call must
+// not re-enter JS with the termination exception still pending. The socket
+// dispatch path calls the error handler when the primary handler throws, and
+// termination cannot be cleared: entering JS again trips Interpreter::
+// executeCallImpl's `assertNoException`. Repro for the
+// test/js/node/test/parallel/test-http2-reset-flood.js SIGABRT.
+import { describe, expect, test } from "bun:test";
+import { bunEnv, bunExe, isWindows } from "harness";
+
+// The handler body shared by both the Bun.listen close handler and the
+// Bun.serve websocket message handler: a two-phase Atomics handshake so the
+// safepoint spin starts only once the parent is already calling terminate(),
+// making the window build-speed-independent.
+//   shared[0]: worker -> parent ("I am inside the handler"; 2 = spin ran out)
+//   shared[1]: parent -> worker ("terminate() is in flight")
+const handlerBody = `
+  Atomics.store(shared, 0, 1);
+  Atomics.notify(shared, 0);
+  Atomics.wait(shared, 1, 0, 5000);
+  // terminate() is now in flight; spin on safepoints so the termination
+  // exception is raised inside this handler frame. Bounded so a missed
+  // terminate cannot hang.
+  let sink = 0;
+  for (let i = 0; i < 10_000_000; i++) sink += Atomics.load(shared, 1);
+  Atomics.store(shared, 0, 2);
+`;
+
+const workerSource = `
+const { parentPort } = require("worker_threads");
+const shared = new Int32Array(require("worker_threads").workerData);
+
+const server = Bun.listen({
+  hostname: "127.0.0.1",
+  port: 0,
+  socket: {
+    open(socket) { socket.write("hello"); },
+    data() {},
+    // socket_body.rs:on_close: a termination raised here returns Err to the
+    // native caller, which then invokes Handlers::call_error_handler.
+    close() {${handlerBody}},
+    error() {},
+  },
+});
+parentPort.postMessage(server.port);
+`;
+
+const wsWorkerSource = `
+const { parentPort } = require("worker_threads");
+const shared = new Int32Array(require("worker_threads").workerData);
+
+const server = Bun.serve({
+  port: 0,
+  fetch(req, server) {
+    if (server.upgrade(req)) return;
+    return new Response("no upgrade", { status: 400 });
+  },
+  websocket: {
+    open(ws) { ws.send("hello"); },
+    // ServerWebSocket.rs:on_message: a termination raised here returns Err to
+    // the native caller, which then invokes WebSocketServerContext::
+    // run_error_callback.
+    message() {${handlerBody}},
+    close() {},
+    error() {},
+  },
+});
+parentPort.postMessage(server.port);
+`;
+
+function parentSource(workerSrc: string, driveHandler: string, cleanup: string) {
+  return `
+const { Worker } = require("worker_threads");
+const net = require("net");
+
+(async () => {
+  // Each iteration is an independent opportunity for terminate() to land inside
+  // the handler. The two-phase handshake makes it land on the first try; a few
+  // repeats leave headroom for CI scheduling jitter.
+  let hits = 0;
+  for (let i = 0; i < 6; i++) {
+    const sab = new SharedArrayBuffer(8);
+    const shared = new Int32Array(sab);
+    const worker = new Worker(${JSON.stringify(workerSrc)}, { eval: true, workerData: sab });
+    const port = await new Promise(resolve => worker.once("message", resolve));
+    ${driveHandler}
+    // Wait until the worker is inside the handler, then release it from its
+    // own wait and terminate so the termination exception lands mid-handler.
+    if (Atomics.wait(shared, 0, 0, 5000) === "timed-out") throw new Error("handler never fired");
+    Atomics.store(shared, 1, 1);
+    Atomics.notify(shared, 1);
+    await worker.terminate();
+    ${cleanup}
+    // shared[0] === 1 means termination landed mid-handler (the spin loop was
+    // interrupted); 2 means the handler returned normally first.
+    if (Atomics.load(shared, 0) === 1) hits++;
+  }
+  if (hits === 0) throw new Error("terminate() never landed inside the handler (0/6)");
+  console.log("ok", hits);
+})();
+`;
+}
+
+// A terminate inside the *open* handler takes a different route back into JS:
+// on_open's error branch runs mark_inactive() -> close_and_detach() ->
+// us_socket_close, which synchronously dispatches on_close.
+const openWorkerSource = `
+const { parentPort } = require("worker_threads");
+const shared = new Int32Array(require("worker_threads").workerData);
+const net = require("net");
+
+const server = net.createServer(socket => {
+  socket.write(Buffer.alloc(1 << 16, "x").toString());
+  ${handlerBody}
+});
+server.listen(0, "127.0.0.1", () => parentPort.postMessage(server.address().port));
+`;
+
+// Same shape for Bun.serve websockets: ServerWebSocket::on_open's error branch
+// calls websocket().close(), which re-enters ServerWebSocket::on_close.
+const wsOpenWorkerSource = `
+const { parentPort } = require("worker_threads");
+const shared = new Int32Array(require("worker_threads").workerData);
+
+const server = Bun.serve({
+  port: 0,
+  fetch(req, server) {
+    if (server.upgrade(req)) return;
+    return new Response("no upgrade", { status: 400 });
+  },
+  websocket: {
+    open() {${handlerBody}},
+    message() {},
+    close() {},
+    error() {},
+  },
+});
+parentPort.postMessage(server.port);
+`;
+
+const listenDriver = `
+    const conn = net.connect({ port, host: "127.0.0.1" });
+    await new Promise(resolve => conn.once("data", resolve));
+    // Closing the client drives on_close on the server's per-connection socket.
+    conn.destroy();
+`;
+
+// The parent must not block in Atomics.wait before the bytes have actually left
+// the socket, or the worker's handler never fires.
+const openDriver = `
+    const conn = net.connect({ port, host: "127.0.0.1" });
+    conn.on("error", () => {});
+    await new Promise(resolve => conn.once("connect", resolve));
+`;
+
+// Raw handshake rather than \`new WebSocket\`: the upgrade has to be flushed
+// before the parent blocks, and the server's open() never lets the client's
+// handshake complete.
+const wsOpenDriver = `
+    const conn = net.connect({ port, host: "127.0.0.1" });
+    conn.on("error", () => {});
+    conn.on("data", () => {});
+    await new Promise(resolve => conn.once("connect", resolve));
+    await new Promise(resolve => conn.write(
+      "GET / HTTP/1.1\\r\\nHost: 127.0.0.1\\r\\nUpgrade: websocket\\r\\nConnection: Upgrade\\r\\n" +
+      "Sec-WebSocket-Key: dGhlIHNhbXBsZSBub25jZQ==\\r\\nSec-WebSocket-Version: 13\\r\\n\\r\\n",
+      resolve,
+    ));
+`;
+
+const wsDriver = `
+    const ws = new WebSocket("ws://127.0.0.1:" + port);
+    await new Promise((resolve, reject) => { ws.onopen = resolve; ws.onerror = reject; });
+    // Terminating the worker ends the connection under the client; swallow the
+    // resulting ErrorEvent so it does not surface as an uncaught error.
+    ws.onerror = () => {};
+    ws.send("go");
+`;
+
+// On Windows the usockets close path and Atomics.wait scheduling differ enough
+// that the window does not open; the bug is platform-agnostic and is exercised
+// on the POSIX lanes.
+describe.skipIf(isWindows)(
+  "worker.terminate() mid-handler does not re-enter JS with a pending termination exception",
+  () => {
+    for (const [name, src] of [
+      ["Bun.listen close handler (socket Handlers::call_error_handler)", parentSource(workerSource, listenDriver, "")],
+      [
+        "Bun.serve websocket message handler (WebSocketServerContext::run_error_callback)",
+        parentSource(wsWorkerSource, wsDriver, "ws.close();"),
+      ],
+      [
+        "node:net connection handler (on_open -> mark_inactive -> on_close)",
+        parentSource(openWorkerSource, openDriver, "conn.destroy();"),
+      ],
+      [
+        "Bun.serve websocket open handler (ServerWebSocket::on_close)",
+        parentSource(wsOpenWorkerSource, wsOpenDriver, "conn.destroy();"),
+      ],
+    ] as const) {
+      test.concurrent(
+        name,
+        async () => {
+          await using proc = Bun.spawn({
+            cmd: [bunExe(), "-e", src],
+            env: bunEnv,
+            stdout: "pipe",
+            stderr: "pipe",
+          });
+          const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+          // The unpatched build aborts inside an iteration (exit 134,
+          // "ASSERTION FAILED: !exception()" on stderr, no stdout). Assert on
+          // stdout/exitCode so benign debug-build stderr noise cannot cause a
+          // false positive; the crash's stderr is in the diff either way.
+          expect({ stdout: stdout.trim(), stderr, exitCode }).toMatchObject({
+            stdout: expect.stringMatching(/^ok [1-6]$/),
+            exitCode: 0,
+          });
+        },
+        60_000,
+      );
+    }
+  },
+);