diff --git a/src/libs/actions/OnyxUpdateManager/index.ts b/src/libs/actions/OnyxUpdateManager/index.ts
index 2a7081009ea3..4bef25f9e8a3 100644
--- a/src/libs/actions/OnyxUpdateManager/index.ts
+++ b/src/libs/actions/OnyxUpdateManager/index.ts
@@ -154,6 +154,13 @@ function handleMissingOnyxUpdates<TKey extends OnyxKey>(onyxUpdatesFromServer: O
     // we don't have base state of the app (reports, policies, etc.) setup. If we apply this update,
     // we'll only have them overwritten by the openApp response. So let's skip it and return.
     if (isLoadingApp) {
+        // If one of these onyx updates is for the authToken, update it now because our current authToken is probably invalid.
+        updateAuthTokenIfNecessary(onyxUpdatesFromServer);
+
+        // Nothing reads this key again once we return, but it is persisted, so a restart would replay it and
+        // could write a now-stale authToken over a newer session. Drop the consumed copy.
+        Onyx.set(ONYXKEYS.ONYX_UPDATES_FROM_SERVER, null);
+
         // When ONYX_UPDATES_FROM_SERVER is set, we pause the queue. Let's unpause
         // it so the app is not stuck forever without processing requests.
         unpauseSequentialQueue();