diff --git a/lib/internal/test_runner/runner.js b/lib/internal/test_runner/runner.js
index 5b2a74c7b62862..c539f6d68af14a 100644
--- a/lib/internal/test_runner/runner.js
+++ b/lib/internal/test_runner/runner.js
@@ -409,8 +409,8 @@ function runTestFile(path, root, inspectPort, filesWatcher, testNamePatterns) {
   return subtest.start();
 }
 
-function watchFiles(testFiles, root, inspectPort, testNamePatterns) {
-  const filesWatcher = new FilesWatcher({ throttle: 500, mode: 'filter' });
+function watchFiles(testFiles, root, inspectPort, signal, testNamePatterns) {
+  const filesWatcher = new FilesWatcher({ throttle: 500, mode: 'filter', signal });
   filesWatcher.on('changed', ({ owners }) => {
     filesWatcher.unfilterFilesOwnedBy(owners);
     PromisePrototypeThen(SafePromiseAllReturnVoid(testFiles, async (file) => {
@@ -432,6 +432,7 @@ function watchFiles(testFiles, root, inspectPort, testNamePatterns) {
       triggerUncaughtException(error, true /* fromPromise */);
     }));
   });
+  signal?.addEventListener('abort', () => root.postRun(), { __proto__: null, once: true });
   return filesWatcher;
 }
 
@@ -474,7 +475,7 @@ function run(options) {
   let postRun = () => root.postRun();
   let filesWatcher;
   if (watch) {
-    filesWatcher = watchFiles(testFiles, root, inspectPort, testNamePatterns);
+    filesWatcher = watchFiles(testFiles, root, inspectPort, signal, testNamePatterns);
     postRun = undefined;
   }
   const runFiles = () => {
diff --git a/lib/internal/watch_mode/files_watcher.js b/lib/internal/watch_mode/files_watcher.js
index 3c756c4b5d77c9..1fa4fc14cd4d4d 100644
--- a/lib/internal/watch_mode/files_watcher.js
+++ b/lib/internal/watch_mode/files_watcher.js
@@ -30,14 +30,18 @@ class FilesWatcher extends EventEmitter {
   #ownerDependencies = new SafeMap();
   #throttle;
   #mode;
+  #signal;
 
-  constructor({ throttle = 500, mode = 'filter' } = kEmptyObject) {
+  constructor({ throttle = 500, mode = 'filter', signal } = kEmptyObject) {
     super();
 
     validateNumber(throttle, 'options.throttle', 0, TIMEOUT_MAX);
     validateOneOf(mode, 'options.mode', ['filter', 'all']);
     this.#throttle = throttle;
     this.#mode = mode;
+    this.#signal = signal;
+
+    signal?.addEventListener('abort', () => this.clear(), { __proto__: null, once: true });
   }
 
   #isPathWatched(path) {
@@ -89,7 +93,7 @@ class FilesWatcher extends EventEmitter {
     if (this.#isPathWatched(path)) {
       return;
     }
-    const watcher = watch(path, { recursive });
+    const watcher = watch(path, { recursive, signal: this.#signal });
     watcher.on('change', (eventType, fileName) => this
       .#onChange(recursive ? resolve(path, fileName) : path));
     this.#watchers.set(path, { handle: watcher, recursive });
diff --git a/test/parallel/test-runner-run.mjs b/test/parallel/test-runner-run.mjs
index 794d55ab1a51d1..866b283981136a 100644
--- a/test/parallel/test-runner-run.mjs
+++ b/test/parallel/test-runner-run.mjs
@@ -117,4 +117,19 @@ describe('require(\'node:test\').run', { concurrency: true }, () => {
     assert.strictEqual(result[2], 'ok 1 - this should be skipped # SKIP test name does not match pattern\n');
     assert.strictEqual(result[5], 'ok 2 - this should be executed\n');
   });
+
+  it('should stop watch mode when abortSignal aborts', async () => {
+    const controller = new AbortController();
+    const result = await run({ files: [join(testFixtures, 'test/random.cjs')], watch: true, signal: controller.signal })
+      .compose(async function* (source) {
+        for await (const chunk of source) {
+          if (chunk.type === 'test:pass') {
+            controller.abort();
+            yield chunk.data.name;
+          }
+        }
+      })
+      .toArray();
+    assert.deepStrictEqual(result, ['this should pass']);
+  });
 });