diff --git a/airflow-core/docs/core-concepts/auth-manager/index.rst b/airflow-core/docs/core-concepts/auth-manager/index.rst
index 98bd93602819a..e07ea5a30c4c5 100644
--- a/airflow-core/docs/core-concepts/auth-manager/index.rst
+++ b/airflow-core/docs/core-concepts/auth-manager/index.rst
@@ -145,7 +145,9 @@ delete the cookie.
     from airflow.api_fastapi.auth.managers.base_auth_manager import COOKIE_NAME_JWT_TOKEN
 
     response = RedirectResponse(url="/")
-    response.set_cookie(COOKIE_NAME_JWT_TOKEN, token, secure=True)
+
+    secure = conf.getboolean("api", "ssl_cert")
+    response.set_cookie(COOKIE_NAME_JWT_TOKEN, token, secure=secure)
     return response
 
 .. note::
diff --git a/airflow-core/src/airflow/api_fastapi/auth/managers/simple/routes/login.py b/airflow-core/src/airflow/api_fastapi/auth/managers/simple/routes/login.py
index b637a12373be3..a9dd3ff6217ff 100644
--- a/airflow-core/src/airflow/api_fastapi/auth/managers/simple/routes/login.py
+++ b/airflow-core/src/airflow/api_fastapi/auth/managers/simple/routes/login.py
@@ -63,10 +63,12 @@ def create_token_all_admins() -> RedirectResponse:
     )
 
     response = RedirectResponse(url=conf.get("api", "base_url"))
+
+    secure = conf.getboolean("api", "ssl_cert")
     response.set_cookie(
         COOKIE_NAME_JWT_TOKEN,
         get_auth_manager().generate_jwt(user),
-        secure=True,
+        secure=secure,
     )
     return response
 
diff --git a/airflow-core/src/airflow/api_fastapi/auth/managers/simple/ui/src/login/Login.tsx b/airflow-core/src/airflow/api_fastapi/auth/managers/simple/ui/src/login/Login.tsx
index e0321ad08e9ad..e9631fbb9d73f 100644
--- a/airflow-core/src/airflow/api_fastapi/auth/managers/simple/ui/src/login/Login.tsx
+++ b/airflow-core/src/airflow/api_fastapi/auth/managers/simple/ui/src/login/Login.tsx
@@ -43,7 +43,7 @@ export const Login = () => {
         // Redirect to appropriate page with the token
         const next = searchParams.get("next")
 
-        setCookie('_token', data.jwt_token, {path: "/", secure: true});
+        setCookie('_token', data.jwt_token, {path: "/", secure: globalThis.location.protocol !== "http:"});
 
         globalThis.location.replace(`${next ?? ""}`);
     }
diff --git a/airflow-core/tests/unit/api_fastapi/auth/managers/simple/routes/test_login.py b/airflow-core/tests/unit/api_fastapi/auth/managers/simple/routes/test_login.py
index 70a39814f2db3..51048a5ba93f5 100644
--- a/airflow-core/tests/unit/api_fastapi/auth/managers/simple/routes/test_login.py
+++ b/airflow-core/tests/unit/api_fastapi/auth/managers/simple/routes/test_login.py
@@ -58,7 +58,7 @@ def test_create_token_invalid_user_password(self, test_client):
         assert response.json()["detail"] == "Invalid credentials"
 
     def test_create_token_all_admins(self, test_client):
-        with conf_vars({("core", "simple_auth_manager_all_admins"): "true"}):
+        with conf_vars({("core", "simple_auth_manager_all_admins"): "true", ("api", "ssl_cert"): "false"}):
             response = test_client.get("/auth/token", follow_redirects=False)
             assert response.status_code == 307
             assert "location" in response.headers
diff --git a/providers/amazon/src/airflow/providers/amazon/aws/auth_manager/router/login.py b/providers/amazon/src/airflow/providers/amazon/aws/auth_manager/router/login.py
index d00ef2e7febdc..b1c771543121b 100644
--- a/providers/amazon/src/airflow/providers/amazon/aws/auth_manager/router/login.py
+++ b/providers/amazon/src/airflow/providers/amazon/aws/auth_manager/router/login.py
@@ -83,7 +83,9 @@ def login_callback(request: Request):
     url = conf.get("api", "base_url")
     token = get_auth_manager().generate_jwt(user)
     response = RedirectResponse(url=url, status_code=303)
-    response.set_cookie(COOKIE_NAME_JWT_TOKEN, token, secure=True)
+
+    secure = conf.getboolean("api", "ssl_cert")
+    response.set_cookie(COOKIE_NAME_JWT_TOKEN, token, secure=secure)
     return response
 
 
diff --git a/providers/amazon/tests/unit/amazon/aws/auth_manager/router/test_login.py b/providers/amazon/tests/unit/amazon/aws/auth_manager/router/test_login.py
index 07c61e32f6723..5f2bdff476661 100644
--- a/providers/amazon/tests/unit/amazon/aws/auth_manager/router/test_login.py
+++ b/providers/amazon/tests/unit/amazon/aws/auth_manager/router/test_login.py
@@ -90,6 +90,7 @@ def test_login_callback_successful(self):
                     "auth_manager",
                 ): "airflow.providers.amazon.aws.auth_manager.aws_auth_manager.AwsAuthManager",
                 ("aws_auth_manager", "saml_metadata_url"): SAML_METADATA_URL,
+                ("api", "ssl_cert"): "false",
             }
         ):
             with (
diff --git a/providers/fab/src/airflow/providers/fab/www/views.py b/providers/fab/src/airflow/providers/fab/www/views.py
index 7a828a7fdfdb1..b14d2eb22c1d8 100644
--- a/providers/fab/src/airflow/providers/fab/www/views.py
+++ b/providers/fab/src/airflow/providers/fab/www/views.py
@@ -70,7 +70,7 @@ def index(self):
             token = get_auth_manager().generate_jwt(g.user)
             response = make_response(redirect(f"{conf.get('api', 'base_url')}", code=302))
 
-            secure = bool(conf.get("api", "ssl_cert"))
+            secure = conf.getboolean("api", "ssl_cert")
             response.set_cookie(COOKIE_NAME_JWT_TOKEN, token, secure=secure)
 
             return response