diff --git a/crates/kernel/src/syscalls.rs b/crates/kernel/src/syscalls.rs
index a027fc1064..fdd97213c1 100644
--- a/crates/kernel/src/syscalls.rs
+++ b/crates/kernel/src/syscalls.rs
@@ -6344,9 +6344,18 @@ pub fn sys_rewinddir(
     let path = stream.path.clone();
     let old_handle = stream.host_handle;
 
-    host.host_closedir(old_handle)?;
+    // Construct the replacement before retiring the current iterator.  A
+    // transient reopen failure must not leave the live DirStream pointing at
+    // a handle that we already closed.
     let new_handle = host.host_opendir(&path)?;
 
+    if let Err(err) = host.host_closedir(old_handle) {
+        // The old iterator remains authoritative when its close fails.  Do
+        // not leak the replacement that never became visible to the stream.
+        let _ = host.host_closedir(new_handle);
+        return Err(err);
+    }
+
     let stream = proc
         .dir_streams
         .get_mut(idx)
@@ -15400,6 +15409,7 @@ mod tests {
         dir_entry_count: usize, // total number of mock entries
         dir_entry_names: Option<Vec<Vec<u8>>>,
         dir_opendir_error: Option<Errno>,
+        dir_closedir_error_once: Option<Errno>,
         dir_readdir_error: Option<(usize, Errno)>,
         sigsuspend_signal: u32,
         sigsuspend_error: bool,
@@ -15466,6 +15476,7 @@ mod tests {
                 dir_entry_count: 1,
                 dir_entry_names: None,
                 dir_opendir_error: None,
+                dir_closedir_error_once: None,
                 dir_readdir_error: None,
                 sigsuspend_signal: 0,
                 sigsuspend_error: false,
@@ -15940,6 +15951,9 @@ mod tests {
         }
 
         fn host_closedir(&mut self, handle: i64) -> Result<(), Errno> {
+            if let Some(err) = self.dir_closedir_error_once.take() {
+                return Err(err);
+            }
             self.dir_entry_indices.remove(&handle);
             self.closed_dir_handles.push(handle);
             Ok(())
@@ -18917,6 +18931,69 @@ mod tests {
         sys_closedir(&mut proc, &mut host, dh).unwrap();
     }
 
+    #[test]
+    fn rewinddir_reopen_failure_preserves_the_live_iterator() {
+        let mut proc = Process::new(1);
+        let mut host = MockHostIO::new();
+        let dh = sys_opendir(&mut proc, &mut host, b"/tmp").unwrap();
+        let original = proc.dir_streams[dh as usize].as_mut().unwrap();
+        original.position = 7;
+        original.synth_dot_state = 2;
+        assert_eq!(original.host_handle, 200);
+
+        host.dir_opendir_error = Some(Errno::EACCES);
+        assert_eq!(
+            sys_rewinddir(&mut proc, &mut host, dh),
+            Err(Errno::EACCES),
+        );
+
+        let preserved = proc.dir_streams[dh as usize].as_ref().unwrap();
+        assert_eq!(preserved.host_handle, 200);
+        assert_eq!(preserved.position, 7);
+        assert_eq!(preserved.synth_dot_state, 2);
+        assert!(host.closed_dir_handles.is_empty());
+
+        host.dir_opendir_error = None;
+        sys_rewinddir(&mut proc, &mut host, dh).unwrap();
+        let rewound = proc.dir_streams[dh as usize].as_ref().unwrap();
+        assert_eq!(rewound.host_handle, 201);
+        assert_eq!(rewound.position, 0);
+        assert_eq!(rewound.synth_dot_state, 0);
+        assert_eq!(host.closed_dir_handles, [200]);
+
+        sys_closedir(&mut proc, &mut host, dh).unwrap();
+        assert_eq!(host.closed_dir_handles, [200, 201]);
+    }
+
+    #[test]
+    fn rewinddir_close_failure_discards_the_replacement() {
+        let mut proc = Process::new(1);
+        let mut host = MockHostIO::new();
+        let dh = sys_opendir(&mut proc, &mut host, b"/tmp").unwrap();
+        let original = proc.dir_streams[dh as usize].as_mut().unwrap();
+        original.position = 7;
+        original.synth_dot_state = 2;
+
+        host.dir_closedir_error_once = Some(Errno::EIO);
+        assert_eq!(sys_rewinddir(&mut proc, &mut host, dh), Err(Errno::EIO));
+
+        let preserved = proc.dir_streams[dh as usize].as_ref().unwrap();
+        assert_eq!(preserved.host_handle, 200);
+        assert_eq!(preserved.position, 7);
+        assert_eq!(preserved.synth_dot_state, 2);
+        assert_eq!(host.closed_dir_handles, [201]);
+
+        sys_rewinddir(&mut proc, &mut host, dh).unwrap();
+        let rewound = proc.dir_streams[dh as usize].as_ref().unwrap();
+        assert_eq!(rewound.host_handle, 202);
+        assert_eq!(rewound.position, 0);
+        assert_eq!(rewound.synth_dot_state, 0);
+        assert_eq!(host.closed_dir_handles, [201, 200]);
+
+        sys_closedir(&mut proc, &mut host, dh).unwrap();
+        assert_eq!(host.closed_dir_handles, [201, 200, 202]);
+    }
+
     #[test]
     fn test_telldir_returns_position() {
         let mut proc = Process::new(1);
diff --git a/docs/posix-status.md b/docs/posix-status.md
index 119710f9ab..be1ad19b5d 100644
--- a/docs/posix-status.md
+++ b/docs/posix-status.md
@@ -214,7 +214,7 @@ to a different directory than the original OFD.
 | `opendir()` | Partial | Host-delegated via DirStream table. Entry-at-a-time iteration. Stores resolved path for rewinddir. |
 | `readdir()` | Full | Returns WasmDirent (d_ino, d_type, d_namlen) + name buffer. Synthesizes "." and ".." entries before host entries. Tracks position for telldir/seekdir. |
 | `closedir()` | Full | Frees DirStream slot, delegates to host. |
-| `rewinddir()` | Full | Closes and reopens directory via stored path. Resets position to 0. |
+| `rewinddir()` | Full | Reopens the directory via its stored path and resets the position to zero. The replacement is opened before the live iterator is retired, so a failed reopen leaves the previous stream and position intact. |
 | `telldir()` | Full | Returns current position counter from DirStream. |
 | `seekdir()` | Full | Rewinds and skips entries to reach target position. |
 | `mkdir()` | Partial | Host-delegated. Relative paths resolved via kernel cwd. umask applied to mode. |
diff --git a/host/src/types.ts b/host/src/types.ts
index 3b04c2982b..32742a5fac 100644
--- a/host/src/types.ts
+++ b/host/src/types.ts
@@ -108,6 +108,10 @@ export interface PlatformIO {
   utimensat(path: string, atimeSec: number, atimeNsec: number, mtimeSec: number, mtimeNsec: number): void;
 
   // Directory iteration
+  /**
+   * Open a directory and return an opaque handle. A handle must not be reused
+   * while its previous directory iterator is still live.
+   */
   opendir(path: string): number;
   /**
    * Return and consume the next entry. If this throws, the iterator must stay
diff --git a/host/test/readdir-atomicity.test.ts b/host/test/readdir-atomicity.test.ts
index 1263c1e67d..df7f9624af 100644
--- a/host/test/readdir-atomicity.test.ts
+++ b/host/test/readdir-atomicity.test.ts
@@ -93,4 +93,97 @@ describe("host readdir retry atomicity", () => {
       ),
     ).toBe("new-iterator");
   });
+
+  it("clears a staged entry even when the backend close fails", () => {
+    const { io, kernel, memory } = createKernelBridge([
+      { name: "old-iterator", type: 8, ino: 1 },
+    ]);
+    io.closedir.mockImplementationOnce(() => {
+      throw new Error("injected close failure");
+    });
+    const bridge = kernel as unknown as {
+      pendingDirectoryEntries: Map<
+        number,
+        { name: string; type: number; ino: number }
+      >;
+      hostReaddir: (
+        handle: bigint,
+        direntPtr: number,
+        namePtr: number,
+        nameLen: number,
+      ) => number;
+      hostClosedir: (handle: bigint) => number;
+    };
+
+    expect(
+      bridge.hostReaddir(7n, memory.buffer.byteLength - 4, 128, 64),
+    ).toBeLessThan(0);
+    expect(bridge.pendingDirectoryEntries.size).toBe(1);
+    expect(bridge.hostClosedir(7n)).toBeLessThan(0);
+    expect(bridge.pendingDirectoryEntries.size).toBe(0);
+    expect(io.closedir).toHaveBeenCalledWith(7);
+  });
+
+  it("drops stale transport state when opendir returns a reused handle", () => {
+    const { io, kernel, memory } = createKernelBridge([
+      { name: "old-iterator", type: 8, ino: 1 },
+      { name: "new-iterator", type: 4, ino: 2 },
+    ]);
+    const bridge = kernel as unknown as {
+      hostOpendir: (pathPtr: number, pathLen: number) => bigint;
+      hostReaddir: (
+        handle: bigint,
+        direntPtr: number,
+        namePtr: number,
+        nameLen: number,
+      ) => number;
+    };
+
+    expect(
+      bridge.hostReaddir(7n, memory.buffer.byteLength - 4, 128, 64),
+    ).toBeLessThan(0);
+
+    new Uint8Array(memory.buffer, 256, 4).set(
+      new TextEncoder().encode("/tmp"),
+    );
+    expect(bridge.hostOpendir(256, 4)).toBe(7n);
+    expect(bridge.hostReaddir(7n, 0, 128, 64)).toBe(1);
+
+    expect(io.opendir).toHaveBeenCalledWith("/tmp");
+    expect(io.readdir).toHaveBeenCalledTimes(2);
+    expect(
+      new TextDecoder().decode(
+        new Uint8Array(memory.buffer, 128, "new-iterator".length),
+      ),
+    ).toBe("new-iterator");
+  });
+
+  it("replays an entry when the name write fails after metadata was written", () => {
+    const entry = { name: "retry-name", type: 8, ino: 42 };
+    const { io, kernel, memory } = createKernelBridge([entry]);
+    const hostReaddir = (
+      kernel as unknown as {
+        hostReaddir: (
+          handle: bigint,
+          direntPtr: number,
+          namePtr: number,
+          nameLen: number,
+        ) => number;
+      }
+    ).hostReaddir.bind(kernel);
+
+    expect(
+      hostReaddir(7n, 0, memory.buffer.byteLength - 2, entry.name.length),
+    ).toBeLessThan(0);
+    expect(new DataView(memory.buffer).getBigUint64(0, true)).toBe(42n);
+    expect(io.readdir).toHaveBeenCalledTimes(1);
+
+    expect(hostReaddir(7n, 0, 128, entry.name.length)).toBe(1);
+    expect(io.readdir).toHaveBeenCalledTimes(1);
+    expect(
+      new TextDecoder().decode(
+        new Uint8Array(memory.buffer, 128, entry.name.length),
+      ),
+    ).toBe(entry.name);
+  });
 });