diff --git a/server/src/main/java/org/opensearch/index/shard/IndexShard.java b/server/src/main/java/org/opensearch/index/shard/IndexShard.java
index 8541a1f5e554b..726a1f0159f3e 100644
--- a/server/src/main/java/org/opensearch/index/shard/IndexShard.java
+++ b/server/src/main/java/org/opensearch/index/shard/IndexShard.java
@@ -339,6 +339,8 @@ Runnable getGlobalCheckpointSyncer() {
     private final boolean isTimeSeriesIndex;
     private final RemoteRefreshSegmentPressureService remoteRefreshSegmentPressureService;
 
+    private final List<ReferenceManager.RefreshListener> internalRefreshListener = new ArrayList<>();
+
     public IndexShard(
         final ShardRouting shardRouting,
         final IndexSettings indexSettings,
@@ -813,6 +815,13 @@ public void relocated(
                 if (syncTranslog) {
                     maybeSync();
                 }
+
+                // Ensures all in-flight remote store operations drain, before we perform the handoff.
+                internalRefreshListener.stream()
+                    .filter(refreshListener -> refreshListener instanceof Closeable)
+                    .map(refreshListener -> (Closeable) refreshListener)
+                    .close();
+
                 // no shard operation permits are being held here, move state from started to relocated
                 assert indexShardOperationPermits.getActiveOperationsCount() == OPERATIONS_BLOCKED
                     : "in-flight operations in progress while moving shard state to relocated";
@@ -3660,7 +3669,7 @@ private EngineConfig newEngineConfig(LongSupplier globalCheckpointSupplier) thro
             }
         };
 
-        final List<ReferenceManager.RefreshListener> internalRefreshListener = new ArrayList<>();
+        internalRefreshListener.clear();
         internalRefreshListener.add(new RefreshMetricUpdater(refreshMetric));
         if (this.checkpointPublisher != null && shardRouting.primary() && indexSettings.isSegRepLocalEnabled()) {
             internalRefreshListener.add(new CheckpointRefreshListener(this, this.checkpointPublisher));