diff --git a/hermes_cli/web_server.py b/hermes_cli/web_server.py
index ccb20c60fc7..583b83b0410 100644
--- a/hermes_cli/web_server.py
+++ b/hermes_cli/web_server.py
@@ -12188,26 +12188,44 @@ async def pty_ws(ws: WebSocket) -> None:
 
     # --- reader task: PTY master → WebSocket ----------------------------
     async def pump_pty_to_ws() -> None:
-        while True:
-            chunk = await loop.run_in_executor(
-                None, bridge.read, _PTY_READ_CHUNK_TIMEOUT
-            )
-            if chunk is None:  # EOF
-                return
-            if not chunk:  # no data this tick; yield control and retry
-                await asyncio.sleep(0)
-                continue
+        try:
+            while True:
+                chunk = await loop.run_in_executor(
+                    None, bridge.read, _PTY_READ_CHUNK_TIMEOUT
+                )
+                if chunk is None:  # EOF
+                    return
+                if not chunk:  # no data this tick; yield control and retry
+                    await asyncio.sleep(0)
+                    continue
+                try:
+                    await ws.send_bytes(chunk)
+                except Exception:
+                    return
+        finally:
+            # The child has exited (EOF) or the send side broke.  Close the
+            # WebSocket so the writer loop's ``ws.receive()`` returns instead
+            # of blocking forever — otherwise, when the browser's socket is
+            # half-open (no FIN delivered, common on macOS/launchd) the
+            # handler never reaches its ``finally`` and the PTY's fds leak.
+            # With dashboard auto-reconnect (#52962) every dropped socket then
+            # stacks a fresh PTY on top of the orphaned one, exhausting fds.
             try:
-                await ws.send_bytes(chunk)
+                await ws.close()
             except Exception:
-                return
+                pass
 
     reader_task = asyncio.create_task(pump_pty_to_ws())
 
     # --- writer loop: WebSocket → PTY master ----------------------------
     try:
         while True:
-            msg = await ws.receive()
+            try:
+                msg = await ws.receive()
+            except RuntimeError:
+                # Raised when ws.receive() is called after the socket is
+                # already disconnected (e.g. closed by the reader task above).
+                break
             msg_type = msg.get("type")
             if msg_type == "websocket.disconnect":
                 break
diff --git a/infographic/pr-54028-pty-fd-leak/infographic.png b/infographic/pr-54028-pty-fd-leak/infographic.png
new file mode 100644
index 00000000000..15eca67af4d
Binary files /dev/null and b/infographic/pr-54028-pty-fd-leak/infographic.png differ
diff --git a/tests/hermes_cli/test_web_server_pty_reconnect.py b/tests/hermes_cli/test_web_server_pty_reconnect.py
index 4f7878f53d0..5a399407084 100644
--- a/tests/hermes_cli/test_web_server_pty_reconnect.py
+++ b/tests/hermes_cli/test_web_server_pty_reconnect.py
@@ -16,6 +16,7 @@ pytestmark = pytest.mark.skipif(
 class _OneFrameBridge:
     def __init__(self):
         self._sent = False
+        self.closed = False
 
     @classmethod
     def spawn(cls, *args, **kwargs):
@@ -34,7 +35,7 @@ class _OneFrameBridge:
         pass
 
     def close(self):
-        pass
+        self.closed = True
 
 
 @pytest.fixture
@@ -128,3 +129,40 @@ def test_fresh_param_ignores_channel_active_session_file(pty_client, monkeypatch
     assert captured["resume"] is None
     assert captured["active_session_file"] == str(active_file)
     assert not active_file.exists()
+
+
+def test_child_eof_closes_socket_and_bridge(pty_client, monkeypatch):
+    """Child EOF must close the WS server-side and reap the PTY.
+
+    Regression for the FD leak (#54028): the reader task hits EOF when the
+    PTY child exits, but if the browser's socket is half-open (no FIN), the
+    writer loop's ``ws.receive()`` would block forever and the PTY fds would
+    never be closed. The reader now closes the WebSocket on EOF so the
+    handler's ``finally`` runs ``bridge.close()``.
+    """
+    ws, client, token = pty_client
+    bridges = []
+
+    class _RecordingBridge(_OneFrameBridge):
+        @classmethod
+        def spawn(cls, *args, **kwargs):
+            b = cls()
+            bridges.append(b)
+            return b
+
+    monkeypatch.setattr(ws.PtyBridge, "spawn", _RecordingBridge.spawn)
+    monkeypatch.setattr(
+        ws, "_resolve_chat_argv", lambda **kw: (["fake-hermes-tui"], None, None)
+    )
+
+    # The client never sends a disconnect of its own — it only reads the one
+    # frame then the server side must tear everything down on child EOF.
+    with client.websocket_connect(_url(token, channel="eof-chan")) as conn:
+        assert conn.receive_bytes() == b"ready"
+        # Server closes the socket after the child EOFs; receiving again
+        # surfaces the close rather than hanging.
+        with pytest.raises(Exception):
+            conn.receive_bytes()
+
+    assert len(bridges) == 1
+    assert bridges[0].closed is True