diff --git a/airflow/cli/commands/local_commands/api_server_command.py b/airflow/cli/commands/local_commands/api_server_command.py
index 4f3fb5ab07e59..6fa2d4330a2df 100644
--- a/airflow/cli/commands/local_commands/api_server_command.py
+++ b/airflow/cli/commands/local_commands/api_server_command.py
@@ -52,6 +52,11 @@ def api_server(args):
     worker_timeout = args.worker_timeout
     proxy_headers = args.proxy_headers
 
+    # Ensure we set this now, so that each subprocess gets the same value
+    from airflow.utils.jwt_signer import get_signing_key
+
+    get_signing_key("api", "auth_jwt_secret")
+
     if args.dev:
         print(f"Starting the API server on port {args.port} and host {args.host} in development mode.")
         log.warning("Running in dev mode, ignoring uvicorn args")