diff --git a/services/companion/java/com/android/server/companion/CompanionDeviceManagerService.java b/services/companion/java/com/android/server/companion/CompanionDeviceManagerService.java
index 1e50c80f0e719..6aea92fbe730c 100644
--- a/services/companion/java/com/android/server/companion/CompanionDeviceManagerService.java
+++ b/services/companion/java/com/android/server/companion/CompanionDeviceManagerService.java
@@ -82,6 +82,7 @@ import android.net.NetworkPolicyManager;
 import android.os.Binder;
 import android.os.Environment;
 import android.os.Handler;
+import android.os.Message;
 import android.os.Parcel;
 import android.os.PowerWhitelistManager;
 import android.os.RemoteCallbackList;
@@ -185,6 +186,7 @@ public class CompanionDeviceManagerService extends SystemService
     private final CompanionDeviceManagerServiceInternal mLocalService = new LocalService(this);
 
     final Handler mMainHandler = Handler.getMain();
+    private final PersistUserStateHandler mUserPersistenceHandler = new PersistUserStateHandler();
     private CompanionDevicePresenceController mCompanionDevicePresenceController;
 
     /**
@@ -366,9 +368,8 @@ public class CompanionDeviceManagerService extends SystemService
 
         final List<AssociationInfo> updatedAssociations =
                 mAssociationStore.getAssociationsForUser(userId);
-        final Map<String, Set<Integer>> usedIdsForUser = getPreviouslyUsedIdsForUser(userId);
-        BackgroundThread.getHandler().post(() ->
-                mPersistentStore.persistStateForUser(userId, updatedAssociations, usedIdsForUser));
+
+        mUserPersistenceHandler.postPersistUserState(userId);
 
         // Notify listeners if ADDED, REMOVED or UPDATED_ADDRESS_CHANGED.
         // Do NOT notify when UPDATED_ADDRESS_UNCHANGED, which means a minor tweak in association's
@@ -381,6 +382,13 @@ public class CompanionDeviceManagerService extends SystemService
         restartBleScan();
     }
 
+    private void persistStateForUser(@UserIdInt int userId) {
+        final List<AssociationInfo> updatedAssociations =
+                mAssociationStore.getAssociationsForUser(userId);
+        final Map<String, Set<Integer>> usedIdsForUser = getPreviouslyUsedIdsForUser(userId);
+        mPersistentStore.persistStateForUser(userId, updatedAssociations, usedIdsForUser);
+    }
+
     private void notifyListeners(
             @UserIdInt int userId, @NonNull List<AssociationInfo> associations) {
         mListeners.broadcast((listener, callbackUserId) -> {
@@ -1349,4 +1357,29 @@ public class CompanionDeviceManagerService extends SystemService
             mService.associationCleanUp(profile);
         }
     }
+
+    /**
+     * This class is dedicated to handling requests to persist user state.
+     */
+    @SuppressLint("HandlerLeak")
+    private class PersistUserStateHandler extends Handler {
+        PersistUserStateHandler() {
+            super(BackgroundThread.get().getLooper());
+        }
+
+        /**
+         * Persists user state unless there is already an outstanding request for the given user.
+         */
+        synchronized void postPersistUserState(@UserIdInt int userId) {
+            if (!hasMessages(userId)) {
+                sendMessage(obtainMessage(userId));
+            }
+        }
+
+        @Override
+        public void handleMessage(@NonNull Message msg) {
+            final int userId = msg.what;
+            persistStateForUser(userId);
+        }
+    }
 }