diff --git a/ipykernel/kernelbase.py b/ipykernel/kernelbase.py
index aceaf3eb9..c24ffd55c 100644
--- a/ipykernel/kernelbase.py
+++ b/ipykernel/kernelbase.py
@@ -418,7 +418,7 @@ async def dispatch_shell(self, msg, /, subshell_id: str | None = None):
         assert msg["header"].get("subshell_id") == subshell_id
 
         if self._supports_kernel_subshells:
-            stream = self.shell_channel_thread.manager.get_subshell_to_shell_channel_socket(
+            stream = self.shell_channel_thread.manager.get_subshell_to_shell_channel_stream(
                 subshell_id
             )
         else:
diff --git a/ipykernel/socket_pair.py b/ipykernel/socket_pair.py
index e2669b8c0..33043e8fc 100644
--- a/ipykernel/socket_pair.py
+++ b/ipykernel/socket_pair.py
@@ -19,12 +19,13 @@ class SocketPair:
     """
 
     from_socket: zmq.Socket[Any]
+    from_stream: ZMQStream | None = None
     to_socket: zmq.Socket[Any]
     to_stream: ZMQStream | None = None
     on_recv_callback: Any
     on_recv_copy: bool
 
-    def __init__(self, context: zmq.Context[Any], name: str):
+    def __init__(self, context: zmq.Context[Any], name: str, from_io_loop: IOLoop | None = None):
         """Initialize the inproc socker pair."""
         self.from_socket = context.socket(zmq.PAIR)
         self.to_socket = context.socket(zmq.PAIR)
@@ -32,8 +33,14 @@ def __init__(self, context: zmq.Context[Any], name: str):
         self.from_socket.bind(address)
         self.to_socket.connect(address)  # Or do I need to do this in another thread?
 
+        # Optional from_stream, only created if from_io_loop is specified.
+        if from_io_loop is not None:
+            self.from_stream = ZMQStream(self.from_socket, from_io_loop)
+
     def close(self):
         """Close the inproc socker pair."""
+        if self.from_stream is not None:
+            self.from_stream.close()
         self.from_socket.close()
 
         if self.to_stream is not None:
diff --git a/ipykernel/subshell.py b/ipykernel/subshell.py
index 911a9521c..32acd5917 100644
--- a/ipykernel/subshell.py
+++ b/ipykernel/subshell.py
@@ -24,7 +24,7 @@ def __init__(
         super().__init__(name=f"subshell-{subshell_id}", **kwargs)
 
         self.shell_channel_to_subshell = SocketPair(context, subshell_id)
-        self.subshell_to_shell_channel = SocketPair(context, subshell_id + "-reverse")
+        self.subshell_to_shell_channel = SocketPair(context, subshell_id + "-reverse", self.io_loop)
 
         # When aborting flag is set, execute_request messages to this subshell will be aborted.
         self.aborting = False
diff --git a/ipykernel/subshell_manager.py b/ipykernel/subshell_manager.py
index 24d683523..61ffe4ee7 100644
--- a/ipykernel/subshell_manager.py
+++ b/ipykernel/subshell_manager.py
@@ -10,6 +10,7 @@
 
 import zmq
 from tornado.ioloop import IOLoop
+from zmq.eventloop.zmqstream import ZMQStream
 
 from .socket_pair import SocketPair
 from .subshell import SubshellThread
@@ -62,7 +63,8 @@ def __init__(
 
         # Inproc socket pair for communication from main thread to shell channel thread.
         # such as for execute_reply messages.
-        self._main_to_shell_channel = SocketPair(self._context, "main-reverse")
+        main_io_loop = IOLoop.current()
+        self._main_to_shell_channel = SocketPair(self._context, "main-reverse", main_io_loop)
         self._main_to_shell_channel.on_recv(
             self._shell_channel_io_loop, self._send_on_shell_channel
         )
@@ -90,14 +92,17 @@ def get_shell_channel_to_subshell_pair(self, subshell_id: str | None) -> SocketP
         with self._lock_cache:
             return self._cache[subshell_id].shell_channel_to_subshell
 
-    def get_subshell_to_shell_channel_socket(self, subshell_id: str | None) -> zmq.Socket[t.Any]:
-        """Return the socket used by a particular subshell or main shell to send
+    def get_subshell_to_shell_channel_stream(self, subshell_id: str | None) -> ZMQStream:
+        """Return the stream used by a particular subshell or main shell to send
         messages to the shell channel.
         """
         if subshell_id is None:
-            return self._main_to_shell_channel.from_socket
-        with self._lock_cache:
-            return self._cache[subshell_id].subshell_to_shell_channel.from_socket
+            from_stream = self._main_to_shell_channel.from_stream
+        else:
+            with self._lock_cache:
+                from_stream = self._cache[subshell_id].subshell_to_shell_channel.from_stream
+        assert from_stream is not None
+        return from_stream
 
     def get_shell_channel_to_subshell_socket(self, subshell_id: str | None) -> zmq.Socket[t.Any]:
         """Return the socket used by the shell channel to send messages to a particular