diff --git a/lib/internal/test_runner/runner.js b/lib/internal/test_runner/runner.js
index 2b622e6be39eb0..700067e0c8a405 100644
--- a/lib/internal/test_runner/runner.js
+++ b/lib/internal/test_runner/runner.js
@@ -444,6 +444,9 @@ function runTestFile(path, filesWatcher, opts) {
       finished(child.stdout, { __proto__: null, signal: t.signal }),
     ]);
 
+    // Close readline interface to prevent memory leak
+    rl.close();
+
     if (watchMode) {
       filesWatcher.runningProcesses.delete(path);
       filesWatcher.runningSubtests.delete(path);
@@ -506,7 +509,7 @@ function watchFiles(testFiles, opts) {
   }
 
   // Watch for changes in current filtered files
-  watcher.on('changed', ({ owners, eventType }) => {
+  const onChanged = ({ owners, eventType }) => {
     if (!opts.hasFiles && (eventType === 'rename' || eventType === 'change')) {
       const updatedTestFiles = createTestFileList(opts.globPatterns, opts.cwd);
       const newFileName = ArrayPrototypeFind(updatedTestFiles, (x) => !ArrayPrototypeIncludes(testFiles, x));
@@ -547,19 +550,29 @@ function watchFiles(testFiles, opts) {
         triggerUncaughtException(error, true /* fromPromise */);
       }));
     }
-  });
+  };
+
+  watcher.on('changed', onChanged);
+
+  // Cleanup function to remove event listener and prevent memory leak
+  const cleanup = () => {
+    watcher.removeListener('changed', onChanged);
+    opts.root.harness.watching = false;
+    opts.root.postRun();
+  };
+
   if (opts.signal) {
     kResistStopPropagation ??= require('internal/event_target').kResistStopPropagation;
     opts.signal.addEventListener(
       'abort',
-      () => {
-        opts.root.harness.watching = false;
-        opts.root.postRun();
-      },
+      cleanup,
       { __proto__: null, once: true, [kResistStopPropagation]: true },
     );
   }
 
+  // Expose cleanup method for proper resource management
+  filesWatcher.cleanup = cleanup;
+
   return filesWatcher;
 }