diff --git a/src/js/node/fs.ts b/src/js/node/fs.ts
index 42cef617b43..76eca9faef1 100644
--- a/src/js/node/fs.ts
+++ b/src/js/node/fs.ts
@@ -1126,12 +1126,20 @@ class Dir {
   }
 
   async *[Symbol.asyncIterator]() {
-    let entries = (this.#entries ??= (await fs.readdir(this.#path, {
-      withFileTypes: true,
-      encoding: this.#options?.encoding,
-      recursive: this.#options?.recursive,
-    })) as DirentType[]);
-    yield* entries;
+    if (this.#handle < 0) throw $ERR_DIR_CLOSED();
+    try {
+      let entries = (this.#entries ??= (await fs.readdir(this.#path, {
+        withFileTypes: true,
+        encoding: this.#options?.encoding,
+        recursive: this.#options?.recursive,
+      })) as DirentType[]);
+      yield* entries;
+    } finally {
+      // Matches Node (lib/internal/fs/dir.js): the iterator always closes the
+      // handle on exit and lets errors (including ERR_DIR_CLOSED from a manual
+      // close inside the loop) propagate out of the iterator.
+      this.closeSync();
+    }
   }
 }
 
diff --git a/test/regression/issue/28894.test.ts b/test/regression/issue/28894.test.ts
new file mode 100644
index 00000000000..a7990bd5f37
--- /dev/null
+++ b/test/regression/issue/28894.test.ts
@@ -0,0 +1,101 @@
+// https://github.com/oven-sh/bun/issues/28894
+// `fs.Dir` async iterator should close the directory handle on exit
+// (natural completion, `break`, or thrown error) to match Node.js.
+import { expect, test } from "bun:test";
+import { tempDir } from "harness";
+import { opendir as opendirPromise } from "node:fs/promises";
+
+test("Dir async iterator closes handle on break", async () => {
+  using dir = tempDir("dir-iter-break", {
+    "a.txt": "",
+    "b.txt": "",
+    "c.txt": "",
+  });
+  const d = await opendirPromise(String(dir));
+
+  const names: string[] = [];
+  for await (const entry of d) {
+    names.push(entry.name);
+    break;
+  }
+  expect(names).toHaveLength(1);
+
+  // The iterator should have closed the handle. A second close must throw.
+  expect(() => d.closeSync()).toThrow("Directory handle was closed");
+});
+
+test("Dir async iterator closes handle on natural completion", async () => {
+  using dir = tempDir("dir-iter-complete", {
+    "x.txt": "",
+    "y.txt": "",
+  });
+  const d = await opendirPromise(String(dir));
+
+  const names: string[] = [];
+  for await (const entry of d) {
+    names.push(entry.name);
+  }
+  expect(names.sort()).toEqual(["x.txt", "y.txt"]);
+
+  expect(() => d.closeSync()).toThrow("Directory handle was closed");
+});
+
+test("Dir async iterator closes handle when body throws", async () => {
+  using dir = tempDir("dir-iter-throw", {
+    "a.txt": "",
+    "b.txt": "",
+  });
+  const d = await opendirPromise(String(dir));
+
+  await expect(
+    (async () => {
+      for await (const _entry of d) {
+        throw new Error("boom");
+      }
+    })(),
+  ).rejects.toThrow("boom");
+
+  expect(() => d.closeSync()).toThrow("Directory handle was closed");
+});
+
+test("Dir async iterator throws ERR_DIR_CLOSED on second iteration after auto-close", async () => {
+  using dir = tempDir("dir-iter-reiter", {
+    "a.txt": "",
+    "b.txt": "",
+  });
+  const d = await opendirPromise(String(dir));
+
+  for await (const _entry of d) {
+    break;
+  }
+
+  // The first iteration auto-closed the handle. A second iteration must
+  // throw ERR_DIR_CLOSED immediately instead of silently re-yielding cached
+  // entries. Matches Node's behavior.
+  await expect(
+    (async () => {
+      for await (const _entry of d) {
+        // unreachable
+      }
+    })(),
+  ).rejects.toThrow("Directory handle was closed");
+});
+
+test("Dir async iterator throws ERR_DIR_CLOSED when user closed manually inside loop", async () => {
+  using dir = tempDir("dir-iter-user-closed", {
+    "a.txt": "",
+  });
+  const d = await opendirPromise(String(dir));
+
+  // Matches Node: when the user closes the handle inside the loop, the
+  // iterator's finally tries to close again and the resulting ERR_DIR_CLOSED
+  // propagates out of the `for await`.
+  await expect(
+    (async () => {
+      for await (const _entry of d) {
+        d.closeSync();
+        break;
+      }
+    })(),
+  ).rejects.toThrow("Directory handle was closed");
+});