diff --git a/lib/internal/vfs/watcher.js b/lib/internal/vfs/watcher.js
index 0f23c1588b17..f6035abfd8be 100644
--- a/lib/internal/vfs/watcher.js
+++ b/lib/internal/vfs/watcher.js
@@ -4,6 +4,7 @@ const {
   ArrayPrototypePush,
   ObjectAssign,
   Promise,
+  PromiseReject,
   PromiseResolve,
   SafeMap,
   SafeSet,
@@ -579,6 +580,7 @@ const kMaxPendingEvents = 1024;
 class VFSWatchAsyncIterable {
   #watcher;
   #closed = false;
+  #abortError = null;
   #pendingEvents = [];
   #pendingResolvers = [];
 
@@ -616,14 +618,21 @@ class VFSWatchAsyncIterable {
       }
     });
 
-    // Handle abort signal - reject pending next() with AbortError
+    // Handle abort signal - reject the next pending next() with AbortError,
+    // then behave like an exhausted iterator, matching native fs.promises.watch.
     if (signal) {
       const onAbort = () => {
         this.#closed = true;
         const err = new AbortError(undefined, { cause: signal.reason });
-        while (this.#pendingResolvers.length > 0) {
+        if (this.#pendingResolvers.length > 0) {
           const { reject } = this.#pendingResolvers.shift();
           reject(err);
+          while (this.#pendingResolvers.length > 0) {
+            const { resolve } = this.#pendingResolvers.shift();
+            resolve({ done: true, value: undefined });
+          }
+        } else {
+          this.#abortError = err;
         }
         this.#watcher.close();
       };
@@ -648,6 +657,12 @@ class VFSWatchAsyncIterable {
    * @returns {Promise<IteratorResult>}
    */
   next() {
+    if (this.#abortError !== null) {
+      const err = this.#abortError;
+      this.#abortError = null;
+      return PromiseReject(err);
+    }
+
     if (this.#closed) {
       return PromiseResolve({ done: true, value: undefined });
     }
diff --git a/test/parallel/test-vfs-watch-abort-signal.js b/test/parallel/test-vfs-watch-abort-signal.js
index 4ceb9f787445..2b62ffe74788 100644
--- a/test/parallel/test-vfs-watch-abort-signal.js
+++ b/test/parallel/test-vfs-watch-abort-signal.js
@@ -28,11 +28,13 @@ const vfs = require('node:vfs');
     setImmediate(() => myVfs.writeFileSync('/file.txt', 'b'));
   }
 
-  // promises.watch with pre-aborted signal resolves done immediately
+  // promises.watch with pre-aborted signal rejects the first next() with
+  // AbortError, matching native fs.promises.watch
   {
     const myVfs = vfs.create();
     myVfs.writeFileSync('/p.txt', 'a');
     const iter = myVfs.promises.watch('/p.txt', { signal: AbortSignal.abort() });
+    await assert.rejects(iter.next(), { name: 'AbortError', code: 'ABORT_ERR' });
     const r = await iter.next();
     assert.strictEqual(r.done, true);
   }