diff --git a/changelogs/fragments/75313-ansible-connection-returns-none.yaml b/changelogs/fragments/75313-ansible-connection-returns-none.yaml
new file mode 100644
index 00000000000..14fbee7cbc4
--- /dev/null
+++ b/changelogs/fragments/75313-ansible-connection-returns-none.yaml
@@ -0,0 +1,3 @@
+---
+bugfixes:
+- ansible-connection - handle errors when passing methods to persistent connection instead of closing connection (https://github.com/ansible-collections/ansible.netcommon/issues/301).
diff --git a/lib/ansible/cli/scripts/ansible_connection_cli_stub.py b/lib/ansible/cli/scripts/ansible_connection_cli_stub.py
index b1ed18c9c69..e3fdac91b8d 100755
--- a/lib/ansible/cli/scripts/ansible_connection_cli_stub.py
+++ b/lib/ansible/cli/scripts/ansible_connection_cli_stub.py
@@ -135,31 +135,36 @@ class ConnectionProcess(object):
 
                 self.exception = None
                 (s, addr) = self.sock.accept()
-                signal.alarm(0)
-                signal.signal(signal.SIGALRM, self.command_timeout)
-                while True:
-                    data = recv_data(s)
-                    if not data:
-                        break
+                try:
+                    signal.alarm(0)
+                    signal.signal(signal.SIGALRM, self.command_timeout)
+                    while True:
+                        data = recv_data(s)
+                        if not data:
+                            break
 
-                    if log_messages:
-                        display.display("jsonrpc request: %s" % data, log_only=True)
+                        if log_messages:
+                            display.display("jsonrpc request: %s" % data, log_only=True)
 
-                    request = json.loads(to_text(data, errors='surrogate_or_strict'))
-                    if request.get('method') == "exec_command" and not self.connection.connected:
-                        self.connection._connect()
+                        request = json.loads(to_text(data, errors='surrogate_or_strict'))
+                        if request.get('method') == "exec_command" and not self.connection.connected:
+                            self.connection._connect()
 
-                    signal.alarm(self.connection.get_option('persistent_command_timeout'))
+                        signal.alarm(self.connection.get_option('persistent_command_timeout'))
 
-                    resp = self.srv.handle_request(data)
-                    signal.alarm(0)
+                        resp = self.srv.handle_request(data)
+                        signal.alarm(0)
 
-                    if log_messages:
-                        display.display("jsonrpc response: %s" % resp, log_only=True)
+                        if log_messages:
+                            display.display("jsonrpc response: %s" % resp, log_only=True)
 
-                    send_data(s, to_bytes(resp))
+                        send_data(s, to_bytes(resp))
 
-                s.close()
+                except Exception as exc:
+                    error = self.srv.make_error(data, to_text(exc))
+                    send_data(s, to_bytes(error))
+                finally:
+                    s.close()
 
         except Exception as e:
             # socket.accept() will raise EINTR if the socket.close() is called
diff --git a/lib/ansible/utils/jsonrpc.py b/lib/ansible/utils/jsonrpc.py
index 2af8bd3581e..95e081a47b7 100644
--- a/lib/ansible/utils/jsonrpc.py
+++ b/lib/ansible/utils/jsonrpc.py
@@ -72,6 +72,24 @@ class JsonRpcServer(object):
 
         return response
 
+    def make_error(self, request, error_msg):
+        """Produce a correct error payload based on request
+
+        This is here to allow a caller to produce an error response with the
+        correct format and response id outside of handle_request, say if an
+        error has occurred before handle_request could be called.
+        """
+        request = json.loads(to_text(request, errors='surrogate_then_replace'))
+
+        setattr(self, '_identifier', request.get('id'))
+
+        error = self.internal_error(data=to_text(error_msg))
+        response = json.dumps(error)
+
+        delattr(self, '_identifier')
+
+        return response
+
     def register(self, obj):
         self._objects.add(obj)