diff --git a/lib/internal/fs/dir.js b/lib/internal/fs/dir.js
index 32050f31ae6d..9c3963d33d92 100644
--- a/lib/internal/fs/dir.js
+++ b/lib/internal/fs/dir.js
@@ -5,6 +5,7 @@ const {
   ArrayPrototypeShift,
   FunctionPrototypeBind,
   ObjectDefineProperties,
+  ObjectHasOwn,
   PromiseReject,
   SymbolAsyncDispose,
   SymbolAsyncIterator,
@@ -350,6 +351,12 @@ function opendir(path, options, callback) {
     encoding: 'utf8',
   });
 
+  // Validate bufferSize before opening the directory. The Dir constructor
+  // validates it too, but an error thrown from opendirCallback can't be caught.
+  if (ObjectHasOwn(options, 'bufferSize')) {
+    validateUint32(options.bufferSize, 'options.bufferSize', true);
+  }
+
   function opendirCallback(error, handle) {
     if (error) {
       callback(error);
diff --git a/test/parallel/test-fs-opendir-invalid-buffersize.js b/test/parallel/test-fs-opendir-invalid-buffersize.js
new file mode 100644
index 000000000000..53ab5bff5f9d
--- /dev/null
+++ b/test/parallel/test-fs-opendir-invalid-buffersize.js
@@ -0,0 +1,36 @@
+'use strict';
+
+// This tests that fs.opendir() and fs.promises.opendir() report an invalid
+// bufferSize to the caller instead of throwing from an internal callback.
+
+const common = require('../common');
+const assert = require('assert');
+const fs = require('fs');
+
+const tmpdir = require('../common/tmpdir');
+tmpdir.refresh();
+
+for (const bufferSize of [-1, 0, 0.5, 1.5, Infinity, NaN]) {
+  const expected = { code: 'ERR_OUT_OF_RANGE', name: 'RangeError' };
+  assert.throws(
+    () => fs.opendir(tmpdir.path, { bufferSize }, common.mustNotCall()),
+    expected,
+  );
+  assert.rejects(fs.promises.opendir(tmpdir.path, { bufferSize }), expected)
+    .then(common.mustCall());
+}
+
+for (const bufferSize of ['', '1', null, undefined]) {
+  const expected = { code: 'ERR_INVALID_ARG_TYPE', name: 'TypeError' };
+  assert.throws(
+    () => fs.opendir(tmpdir.path, { bufferSize }, common.mustNotCall()),
+    expected,
+  );
+  assert.rejects(fs.promises.opendir(tmpdir.path, { bufferSize }), expected)
+    .then(common.mustCall());
+}
+
+// A valid bufferSize still opens the directory.
+fs.opendir(tmpdir.path, { bufferSize: 1 }, common.mustSucceed((dir) => {
+  dir.closeSync();
+}));