diff --git a/CHANGELOG.md b/CHANGELOG.md
index 6390aa65b..e3d5ab070 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -8,6 +8,7 @@ This project adheres to [Semantic Versioning](http://semver.org/).
 ### Fixed
 
  - #3498, Fix incorrect parsing of the `for` parameter of the `application/vnd.pgrst.plan` media type - @taimoorzaeem
+ - #4014, Fix JWT cache allows old tokens after the jwt-secret is changed in a config reload - @taimoorzaeem
 
 ## [12.2.8] - 2025-02-10
 
diff --git a/src/PostgREST/AppState.hs b/src/PostgREST/AppState.hs
index 43b154b51..1f541955e 100644
--- a/src/PostgREST/AppState.hs
+++ b/src/PostgREST/AppState.hs
@@ -440,11 +440,11 @@ retryingSchemaCacheLoad appState@AppState{stateObserver=observer, stateMainThrea
 -- | We don't retry reading the in-db config after it fails immediately, because it could have user errors. We just report the error and continue.
 readInDbConfig :: Bool -> AppState -> IO ()
 readInDbConfig startingUp appState@AppState{stateObserver=observer} = do
-  AppConfig{..} <- getConfig appState
+  conf <- getConfig appState
   pgVer <- getPgVersion appState
   dbSettings <-
-    if configDbConfig then do
-      qDbSettings <- usePool appState (queryDbSettings (dumpQi <$> configDbPreConfig) configDbPreparedStatements)
+    if configDbConfig conf then do
+      qDbSettings <- usePool appState (queryDbSettings (dumpQi <$> configDbPreConfig conf) (configDbPreparedStatements conf))
       case qDbSettings of
         Left e -> do
           observer $ ConfigReadErrorObs e
@@ -453,8 +453,8 @@ readInDbConfig startingUp appState@AppState{stateObserver=observer} = do
     else
       pure mempty
   (roleSettings, roleIsolationLvl) <-
-    if configDbConfig then do
-      rSettings <- usePool appState (queryRoleSettings pgVer configDbPreparedStatements)
+    if configDbConfig conf then do
+      rSettings <- usePool appState (queryRoleSettings pgVer (configDbPreparedStatements conf))
       case rSettings of
         Left e -> do
           observer $ QueryRoleSettingsErrorObs e
@@ -462,7 +462,7 @@ readInDbConfig startingUp appState@AppState{stateObserver=observer} = do
         Right x -> pure x
     else
       pure mempty
-  readAppConfig dbSettings configFilePath (Just configDbUri) roleSettings roleIsolationLvl >>= \case
+  readAppConfig dbSettings (configFilePath conf) (Just $ configDbUri conf) roleSettings roleIsolationLvl >>= \case
     Left err   ->
       if startingUp then
         panic err -- die on invalid config if the program is starting up
@@ -470,6 +470,14 @@ readInDbConfig startingUp appState@AppState{stateObserver=observer} = do
         observer $ ConfigInvalidObs err
     Right newConf -> do
       putConfig appState newConf
+      -- After the config has reloaded, jwt-secret might have changed, so
+      -- if it has changed, it is important to invalidate the jwt cache
+      -- entries, because they were cached using the old secret
+      if configJwtSecret conf == configJwtSecret newConf then
+        pass
+      else
+        C.purge (getJwtCache appState) -- atomic O(1) operation
+
       if startingUp then
         pass
       else
diff --git a/test/io/test_io.py b/test/io/test_io.py
index f6c479a4b..b60f980b1 100644
--- a/test/io/test_io.py
+++ b/test/io/test_io.py
@@ -1663,3 +1663,38 @@ def test_pgrst_log_503_client_error_to_stderr(defaultenv):
         log_message = '{"code":"PGRST001","details":"no connection to the server\\n","hint":null,"message":"Database client error. Retrying the connection."}\n'
 
         assert any(log_message in line for line in output)
+
+
+def test_invalidate_jwt_cache_when_secret_changes(tmp_path, defaultenv):
+    "JWT cache should be emptied after jwt-secret is changed in a config reload"
+
+    headers = jwtauthheader({"role": "postgrest_test_author"}, SECRET)
+
+    external_secret_file = tmp_path / "jwt-secret-config"
+    external_secret_file.write_text(SECRET)
+
+    env = {
+        **defaultenv,
+        "PGRST_JWT_SECRET": f"@{external_secret_file}",
+        "PGRST_DB_CHANNEL_ENABLED": "true",
+        "PGRST_JWT_CACHE_MAX_LIFETIME": "86400",  # enable cache
+        "PGRST_DB_ANON_ROLE": "postgrest_test_anonymous",  # required for NOTIFY
+    }
+
+    with run(env=env) as postgrest:
+        response = postgrest.session.get("/authors_only", headers=headers)
+        assert response.status_code == 200  # jwt gets cached
+
+        # change external file
+        external_secret_file.write_text("invalid" * 5)
+
+        # reload config and external file with NOTIFY
+        # jwt-cache should get empty
+        response = postgrest.session.post("/rpc/reload_pgrst_config")
+        assert response.text == ""
+        assert response.status_code == 204
+        sleep_until_postgrest_config_reload()
+
+        # now the request should fail because the cached token is removed
+        response = postgrest.session.get("/authors_only", headers=headers)
+        assert response.status_code == 401