diff --git a/lib/internal/fs/streams.js b/lib/internal/fs/streams.js
index 4c53f7ea23e1..3709bb86888b 100644
--- a/lib/internal/fs/streams.js
+++ b/lib/internal/fs/streams.js
@@ -51,6 +51,7 @@ const kIsPerformingIO = Symbol('kIsPerformingIO');
 
 const kFs = Symbol('kFs');
 const kHandle = Symbol('kHandle');
+const kReleaseHandleRef = Symbol('kReleaseHandleRef');
 
 function _construct(callback) {
   const stream = this;
@@ -90,13 +91,13 @@ function _construct(callback) {
 }
 
 // This generates an fs operations structure for a FileHandle
-const FileHandleOperations = (handle) => {
+const FileHandleOperations = (handle, releaseHandleRef) => {
   return {
     open: (path, flags, mode, cb) => {
       throw new ERR_METHOD_NOT_IMPLEMENTED('open()');
     },
     close: (fd, cb) => {
-      handle[kUnref]();
+      releaseHandleRef();
       PromisePrototypeThen(handle.close(),
                            () => cb(), cb);
     },
@@ -155,11 +156,32 @@ function importFd(stream, options) {
       // FileHandle is not supported with custom fs operations
       throw new ERR_METHOD_NOT_IMPLEMENTED('FileHandle with fs');
     }
-    stream[kHandle] = options.fd;
-    stream[kFs] = FileHandleOperations(stream[kHandle]);
-    stream[kHandle][kRef]();
-    options.fd.on('close', FunctionPrototypeBind(stream.close, stream));
-    return options.fd.fd;
+    const handle = options.fd;
+    stream[kHandle] = handle;
+    handle[kRef]();
+
+    // Release the ref/listener exactly once, whichever comes first: the
+    // stream being destroyed (FileHandleOperations.close(), below) or, for
+    // `autoClose: false` streams that finish without ever being destroyed,
+    // finished() below (see willEmitClose() in internal/streams/utils.js).
+    let handleRefReleased = false;
+    const onHandleClose = FunctionPrototypeBind(stream.close, stream);
+    function releaseHandleRef() {
+      if (handleRefReleased) return;
+      handleRefReleased = true;
+      handle.removeListener('close', onHandleClose);
+      handle[kUnref]();
+    }
+
+    stream[kFs] = FileHandleOperations(handle, releaseHandleRef);
+    handle.on('close', onHandleClose);
+    // finished() needs the stream's readable/writable state, which isn't
+    // initialized until Readable.call()/Writable.call() runs later in the
+    // constructor, so defer registering it until then (see kReleaseHandleRef
+    // below).
+    stream[kReleaseHandleRef] = releaseHandleRef;
+
+    return handle.fd;
   }
 
   throw new ERR_INVALID_ARG_TYPE('options.fd',
@@ -255,6 +277,10 @@ function ReadStream(path, options) {
   }
 
   FunctionPrototypeCall(Readable, this, options);
+
+  if (this[kReleaseHandleRef]) {
+    finished(this, this[kReleaseHandleRef]);
+  }
 }
 ObjectSetPrototypeOf(ReadStream.prototype, Readable.prototype);
 ObjectSetPrototypeOf(ReadStream, Readable);
@@ -425,6 +451,10 @@ function WriteStream(path, options) {
 
   if (options.encoding)
     this.setDefaultEncoding(options.encoding);
+
+  if (this[kReleaseHandleRef]) {
+    finished(this, this[kReleaseHandleRef]);
+  }
 }
 ObjectSetPrototypeOf(WriteStream.prototype, Writable.prototype);
 ObjectSetPrototypeOf(WriteStream, Writable);
diff --git a/test/parallel/test-fs-promises-file-handle-stream.js b/test/parallel/test-fs-promises-file-handle-stream.js
index 71f312b6f9d7..9a2bbebc71be 100644
--- a/test/parallel/test-fs-promises-file-handle-stream.js
+++ b/test/parallel/test-fs-promises-file-handle-stream.js
@@ -42,7 +42,133 @@ async function validateRead() {
   );
 }
 
+// Regression test for https://github.com/nodejs/node/issues/64214: every
+// createReadStream({ autoClose: false }) call used to leave behind a 'close'
+// listener on the FileHandle (and an un-released internal ref), because
+// autoClose: false disables autoDestroy, so the stream never goes through
+// _destroy() when it finishes on its own. Repeating this past 10 iterations
+// used to trigger a MaxListenersExceededWarning.
+async function validateReadStreamAutoCloseFalseReleasesListener() {
+  const filePathForHandle = path.resolve(tmpDir, 'tmp-read-autoclose-false.txt');
+  const buf = Buffer.from('Hello world', 'utf8');
+
+  fs.writeFileSync(filePathForHandle, buf);
+
+  const fileHandle = await open(filePathForHandle);
+  try {
+    for (let i = 0; i < buf.length; i++) {
+      const chunk = await buffer(fileHandle.createReadStream({
+        start: i,
+        end: i,
+        autoClose: false,
+      }));
+      assert.strictEqual(chunk[0], buf[i]);
+      assert.strictEqual(fileHandle.listenerCount('close'), 0);
+    }
+  } finally {
+    await fileHandle.close();
+  }
+}
+
+// Same leak, but for createWriteStream({ autoClose: false }).
+async function validateWriteStreamAutoCloseFalseReleasesListener() {
+  const filePathForHandle =
+    path.resolve(tmpDir, 'tmp-write-autoclose-false.txt');
+  const buf = Buffer.from('Hello world', 'utf8');
+
+  const fileHandle = await open(filePathForHandle, 'w');
+  try {
+    for (let i = 0; i < buf.length; i++) {
+      const stream = fileHandle.createWriteStream({
+        start: i,
+        autoClose: false,
+      });
+      stream.end(buf.subarray(i, i + 1));
+      await finished(stream);
+      assert.strictEqual(fileHandle.listenerCount('close'), 0);
+    }
+  } finally {
+    await fileHandle.close();
+  }
+
+  assert.deepStrictEqual(fs.readFileSync(filePathForHandle), buf);
+}
+
+// Regression test for the fix that was reverted in
+// https://github.com/nodejs/node/pull/65387: a previous attempt released the
+// FileHandle ref both when the stream finished on its own *and* again when
+// the stream was explicitly closed/destroyed afterwards, unreffing the
+// handle twice for a single stream. Explicitly closing a stream after it has
+// already finished on its own (autoClose: false) is a normal thing to do and
+// must not double-release the handle's reference count.
+async function validateAutoCloseFalseExplicitCloseDoesNotDoubleRelease() {
+  const filePathForHandle =
+    path.resolve(tmpDir, 'tmp-read-autoclose-false-explicit-close.txt');
+  const buf = Buffer.from('Hello world', 'utf8');
+
+  fs.writeFileSync(filePathForHandle, buf);
+
+  const fileHandle = await open(filePathForHandle);
+  // Register this before anything closes the handle: FileHandleOperations
+  // .close() unconditionally closes the handle once the stream is
+  // destroyed (that's how `autoClose: true` implicitly closes the handle),
+  // so the explicit stream.close() below is expected to trigger it. This
+  // listener itself accounts for one 'close' listener throughout, on top of
+  // whatever the stream adds/removes.
+  const closed = new Promise((resolve) => {
+    fileHandle.once('close', common.mustCall(resolve));
+  });
+
+  const stream = fileHandle.createReadStream({
+    start: 0,
+    end: 0,
+    autoClose: false,
+  });
+  await buffer(stream);
+  // Only the listener registered above remains; the stream's own listener
+  // was released when it finished on its own.
+  assert.strictEqual(fileHandle.listenerCount('close'), 1);
+
+  // The stream already finished on its own (which already released its
+  // handle ref); closing it again must be a safe no-op with respect to that
+  // ref, and must not corrupt the handle's internal reference count.
+  await new Promise((resolve, reject) => {
+    stream.close((err) => (err ? reject(err) : resolve()));
+  });
+  await closed;
+  assert.strictEqual(fileHandle.listenerCount('close'), 0);
+
+  // The handle is already fully closed at this point; closing it again must
+  // remain a safe, immediately-resolving no-op (it would hang or throw if
+  // the ref count had gone negative).
+  await fileHandle.close();
+}
+
+// The default (autoClose: true) behavior must be unaffected: finishing the
+// stream still implicitly closes the FileHandle exactly once, and leaves no
+// listener behind.
+async function validateAutoCloseTrueStillClosesFileHandle() {
+  const filePathForHandle =
+    path.resolve(tmpDir, 'tmp-read-autoclose-true.txt');
+  const buf = Buffer.from('Hello world', 'utf8');
+
+  fs.writeFileSync(filePathForHandle, buf);
+
+  const fileHandle = await open(filePathForHandle);
+  const closed = new Promise((resolve) => {
+    fileHandle.once('close', common.mustCall(resolve));
+  });
+
+  assert.deepStrictEqual(await buffer(fileHandle.createReadStream()), buf);
+  await closed;
+  assert.strictEqual(fileHandle.listenerCount('close'), 0);
+}
+
 Promise.all([
   validateWrite(),
   validateRead(),
+  validateReadStreamAutoCloseFalseReleasesListener(),
+  validateWriteStreamAutoCloseFalseReleasesListener(),
+  validateAutoCloseFalseExplicitCloseDoesNotDoubleRelease(),
+  validateAutoCloseTrueStillClosesFileHandle(),
 ]).then(common.mustCall());