diff --git a/quickwit/quickwit-ingest/src/ingest_v2/router.rs b/quickwit/quickwit-ingest/src/ingest_v2/router.rs
index ecf5f707642..2b19ad497e2 100644
--- a/quickwit/quickwit-ingest/src/ingest_v2/router.rs
+++ b/quickwit/quickwit-ingest/src/ingest_v2/router.rs
@@ -35,7 +35,7 @@ use quickwit_proto::ingest::router::{
     IngestFailureReason, IngestRequestV2, IngestResponseV2, IngestRouterService,
 };
 use quickwit_proto::ingest::{CommitTypeV2, IngestV2Error, IngestV2Result, RateLimitingCause};
-use quickwit_proto::types::{NodeId, SubrequestId};
+use quickwit_proto::types::{IndexUid, NodeId, SourceId, SubrequestId};
 use serde_json::{Value as JsonValue, json};
 use tokio::sync::{Mutex, Semaphore};
 use tokio::time::error::Elapsed;
@@ -286,6 +286,7 @@ impl IngestRouter {
             match persist_result {
                 Ok(persist_response) => {
                     let leader_id = NodeId::from_str(&persist_response.leader_id);
+                    let mut no_shards_entries: Vec<(IndexUid, SourceId)> = Vec::new();
 
                     for persist_success in persist_response.successes {
                         workbench.record_persist_success(persist_success);
@@ -295,9 +296,18 @@ impl IngestRouter {
 
                         match persist_failure.reason() {
                             PersistFailureReason::NoShardsAvailable => {
-                                // For non-critical failures, we don't mark the nodes unavailable;
-                                // a routing update is piggybacked on PersistResponses, so shard
-                                // counts and capacity scores will be fresh on the next try.
+                                // The ingester reported no shard for this (index_uid,
+                                // source_id). The piggybacked routing update only covers
+                                // sources the ingester still holds, so a removed source
+                                // (e.g. after an index was deleted and recreated) would
+                                // leave this node's entry stale and trap retries on a
+                                // dead shard. Mark the node as having zero open shards
+                                // for this entry; when no nodes remain, the next attempt
+                                // re-queries the control plane.
+                                no_shards_entries.push((
+                                    persist_failure.index_uid().clone(),
+                                    persist_failure.source_id.clone(),
+                                ));
                             }
                             PersistFailureReason::NodeUnavailable
                             | PersistFailureReason::WalFull
@@ -308,22 +318,35 @@ impl IngestRouter {
                         }
                     }
 
-                    if let Some(routing_update) = persist_response.routing_update {
+                    if !no_shards_entries.is_empty() || persist_response.routing_update.is_some() {
                         // Since we just talked to the node, we take advantage and use the
-                        // opportunity to get a fresh routing update.
+                        // opportunity to get a fresh routing update. Both the zero-out and the
+                        // piggybacked update run under the same lock so the rate-limited
+                        // subcase of NoShardsAvailable — where the shard still exists — is
+                        // immediately restored by the routing update that follows (the ingester
+                        // only returns routing_update=None on the NodeUnavailable fast path).
                         let mut state_guard = self.state.lock().await;
-                        for shard_update in routing_update.source_shard_updates {
-                            state_guard.routing_table.apply_capacity_update(
-                                leader_id.clone(),
-                                shard_update.index_uid().clone(),
-                                shard_update.source_id,
-                                routing_update.capacity_score as usize,
-                                shard_update.open_shard_count as usize,
-                            );
+
+                        for (index_uid, source_id) in &no_shards_entries {
+                            state_guard
+                                .routing_table
+                                .mark_node_no_shards(&leader_id, index_uid, source_id);
                         }
-                        drop(state_guard);
 
-                        workbench.closed_shards.extend(routing_update.closed_shards);
+                        if let Some(routing_update) = persist_response.routing_update {
+                            for shard_update in routing_update.source_shard_updates {
+                                state_guard.routing_table.apply_capacity_update(
+                                    leader_id.clone(),
+                                    shard_update.index_uid().clone(),
+                                    shard_update.source_id,
+                                    routing_update.capacity_score as usize,
+                                    shard_update.open_shard_count as usize,
+                                );
+                            }
+                            drop(state_guard);
+
+                            workbench.closed_shards.extend(routing_update.closed_shards);
+                        }
                     }
                 }
                 Err(persist_error) => {
@@ -1860,4 +1883,190 @@ mod tests {
             .unwrap();
         assert_eq!(node.node_id, NodeId::from_str("test-ingester-0"));
     }
+
+    #[tokio::test]
+    async fn test_no_shards_available_clears_stale_routing_entry() {
+        // Regression test for https://github.com/quickwit-oss/quickwit/issues/6324.
+        //
+        // When an index is deleted and recreated, the ingester closes its old shards and
+        // stops advertising them. A persist request issued against the stale routing
+        // entry fails with NoShardsAvailable, and the piggybacked routing update no
+        // longer covers the removed source — so before the fix the router kept picking
+        // the dead entry forever and ingests returned 503 until Chitchat caught up.
+        let ingester_pool = IngesterPool::default();
+        let router = IngestRouter::new(
+            "test-router".into(),
+            ControlPlaneServiceClient::from_mock(MockControlPlaneService::new()),
+            ingester_pool.clone(),
+            1,
+            EventBroker::default(),
+            Some("test-az".to_string()),
+        );
+        let stale_index_uid = IndexUid::for_test("test-index", 0);
+        {
+            let mut state_guard = router.state.lock().await;
+            state_guard.routing_table.merge_from_shards(
+                stale_index_uid.clone(),
+                "test-source".to_string(),
+                vec![Shard {
+                    index_uid: Some(stale_index_uid.clone()),
+                    source_id: "test-source".to_string(),
+                    shard_id: Some(ShardId::from(1)),
+                    shard_state: ShardState::Open as i32,
+                    leader_id: "test-ingester-0".to_string(),
+                    ..Default::default()
+                }],
+            );
+        }
+        ingester_pool.insert(
+            "test-ingester-0".into(),
+            IngesterPoolEntry::mocked_ingester(),
+        );
+
+        // Sanity-check: the stale entry is currently considered valid for routing.
+        {
+            let state_guard = router.state.lock().await;
+            let mut unavailable_leaders: HashSet<NodeId> = HashSet::new();
+            assert!(state_guard.routing_table.has_any_routing_candidate(
+                "test-index",
+                "test-source",
+                &ingester_pool,
+                &mut unavailable_leaders,
+            ));
+        }
+
+        let ingest_subrequests = vec![IngestSubrequest {
+            subrequest_id: 0,
+            index_id: "test-index".to_string(),
+            source_id: "test-source".to_string(),
+            ..Default::default()
+        }];
+        let mut workbench = IngestWorkbench::new(ingest_subrequests, 2);
+
+        let persist_futures = FuturesUnordered::new();
+        let stale_index_uid_clone = stale_index_uid.clone();
+        persist_futures.push(async move {
+            let summary = PersistRequestSummary {
+                leader_id: "test-ingester-0".into(),
+                subrequest_ids: vec![0],
+            };
+            let result = Ok::<_, IngestV2Error>(PersistResponse {
+                leader_id: "test-ingester-0".to_string(),
+                successes: Vec::new(),
+                failures: vec![PersistFailure {
+                    subrequest_id: 0,
+                    index_uid: Some(stale_index_uid_clone),
+                    source_id: "test-source".to_string(),
+                    reason: PersistFailureReason::NoShardsAvailable as i32,
+                }],
+                // The ingester has no shard for this source anymore, so the piggybacked
+                // routing update omits it entirely.
+                routing_update: Some(RoutingUpdate {
+                    capacity_score: 6,
+                    source_shard_updates: Vec::new(),
+                    ..Default::default()
+                }),
+            });
+            (summary, result)
+        });
+        router
+            .process_persist_results(&mut workbench, persist_futures)
+            .await;
+
+        // The stale routing entry must no longer look routable — otherwise retries would
+        // keep hammering the dead shard and surface as a 503.
+        let state_guard = router.state.lock().await;
+        let mut unavailable_leaders: HashSet<NodeId> = HashSet::new();
+        assert!(!state_guard.routing_table.has_any_routing_candidate(
+            "test-index",
+            "test-source",
+            &ingester_pool,
+            &mut unavailable_leaders,
+        ));
+    }
+
+    #[tokio::test]
+    async fn test_no_shards_available_preserves_entry_when_routing_update_refreshes_it() {
+        // When a shard is merely rate-limited the ingester still returns NoShardsAvailable
+        // but includes a fresh routing update saying the shard is open. The update must
+        // take precedence so the node remains routable for the next retry.
+        let ingester_pool = IngesterPool::default();
+        let router = IngestRouter::new(
+            "test-router".into(),
+            ControlPlaneServiceClient::from_mock(MockControlPlaneService::new()),
+            ingester_pool.clone(),
+            1,
+            EventBroker::default(),
+            Some("test-az".to_string()),
+        );
+        let index_uid = IndexUid::for_test("test-index", 0);
+        {
+            let mut state_guard = router.state.lock().await;
+            state_guard.routing_table.merge_from_shards(
+                index_uid.clone(),
+                "test-source".to_string(),
+                vec![Shard {
+                    index_uid: Some(index_uid.clone()),
+                    source_id: "test-source".to_string(),
+                    shard_id: Some(ShardId::from(1)),
+                    shard_state: ShardState::Open as i32,
+                    leader_id: "test-ingester-0".to_string(),
+                    ..Default::default()
+                }],
+            );
+        }
+        ingester_pool.insert(
+            "test-ingester-0".into(),
+            IngesterPoolEntry::mocked_ingester(),
+        );
+
+        let ingest_subrequests = vec![IngestSubrequest {
+            subrequest_id: 0,
+            index_id: "test-index".to_string(),
+            source_id: "test-source".to_string(),
+            ..Default::default()
+        }];
+        let mut workbench = IngestWorkbench::new(ingest_subrequests, 2);
+
+        let persist_futures = FuturesUnordered::new();
+        let index_uid_clone = index_uid.clone();
+        persist_futures.push(async move {
+            let summary = PersistRequestSummary {
+                leader_id: "test-ingester-0".into(),
+                subrequest_ids: vec![0],
+            };
+            let result = Ok::<_, IngestV2Error>(PersistResponse {
+                leader_id: "test-ingester-0".to_string(),
+                successes: Vec::new(),
+                failures: vec![PersistFailure {
+                    subrequest_id: 0,
+                    index_uid: Some(index_uid_clone.clone()),
+                    source_id: "test-source".to_string(),
+                    reason: PersistFailureReason::NoShardsAvailable as i32,
+                }],
+                routing_update: Some(RoutingUpdate {
+                    capacity_score: 6,
+                    source_shard_updates: vec![SourceShardUpdate {
+                        index_uid: Some(index_uid_clone),
+                        source_id: "test-source".to_string(),
+                        open_shard_count: 1,
+                    }],
+                    ..Default::default()
+                }),
+            });
+            (summary, result)
+        });
+        router
+            .process_persist_results(&mut workbench, persist_futures)
+            .await;
+
+        let state_guard = router.state.lock().await;
+        let mut unavailable_leaders: HashSet<NodeId> = HashSet::new();
+        assert!(state_guard.routing_table.has_any_routing_candidate(
+            "test-index",
+            "test-source",
+            &ingester_pool,
+            &mut unavailable_leaders,
+        ));
+    }
 }
diff --git a/quickwit/quickwit-ingest/src/ingest_v2/routing_table.rs b/quickwit/quickwit-ingest/src/ingest_v2/routing_table.rs
index 973de0e582a..0aed8b33663 100644
--- a/quickwit/quickwit-ingest/src/ingest_v2/routing_table.rs
+++ b/quickwit/quickwit-ingest/src/ingest_v2/routing_table.rs
@@ -273,6 +273,36 @@ impl RoutingTable {
         entry.nodes.insert(node_id, ingester_node);
     }
 
+    /// Zeros out the open shard count for `node_id` on the (index, source) entry while preserving
+    /// its capacity score. Called when a persist response reports that the ingester no longer
+    /// holds a shard for this (index_uid, source_id), so the entry stops being picked until a
+    /// fresh routing update or control-plane response repopulates it.
+    ///
+    /// Mirrors the incarnation handling of [`Self::apply_capacity_update`]: a stale signal
+    /// (entry newer than `index_uid`) is ignored, and a signal for a newer incarnation advances
+    /// the entry and clears stale nodes so the next attempt re-queries the control plane.
+    pub fn mark_node_no_shards(&mut self, node_id: &NodeId, index_uid: &IndexUid, source_id: &str) {
+        let key = (index_uid.index_id.to_string(), source_id.to_string());
+        let Some(entry) = self.table.get_mut(&key) else {
+            return;
+        };
+        match entry.index_uid.cmp(index_uid) {
+            // The entry is stale relative to the signal: advance it, drop stale nodes, and force
+            // a control-plane re-seed on the next attempt.
+            Ordering::Less => {
+                entry.index_uid = index_uid.clone();
+                entry.nodes.clear();
+                entry.seeded_from_cp = false;
+            }
+            // The signal is stale relative to the entry: leave the fresher entry alone.
+            Ordering::Greater => return,
+            Ordering::Equal => {}
+        }
+        if let Some(node) = entry.nodes.get_mut(node_id) {
+            node.open_shard_count = 0;
+        }
+    }
+
     /// Merges routing updates from a GetOrCreateOpenShards control plane response into the
     /// table. For existing nodes, updates their open shard count, including if the count is 0, from
     /// the CP response while preserving capacity scores if they already exist.
@@ -856,4 +886,73 @@ mod tests {
         assert!(!entry.nodes.contains_key("node-3"));
         assert_eq!(entry.index_uid, IndexUid::for_test("test-index", 2));
     }
+
+    #[test]
+    fn test_mark_node_no_shards() {
+        let mut table = RoutingTable::default();
+        let index_uid = IndexUid::for_test("test-index", 1);
+        let key = ("test-index".to_string(), "test-source".to_string());
+
+        // Missing entry: no-op, no panic, nothing inserted.
+        table.mark_node_no_shards(&"node-1".into(), &index_uid, "test-source");
+        assert!(table.table.get(&key).is_none());
+
+        // Seed an entry with two nodes carrying real capacity scores.
+        table.apply_capacity_update(
+            "node-1".into(),
+            index_uid.clone(),
+            "test-source".into(),
+            8,
+            3,
+        );
+        table.apply_capacity_update(
+            "node-2".into(),
+            index_uid.clone(),
+            "test-source".into(),
+            6,
+            2,
+        );
+
+        // Missing node within the entry: no-op.
+        table.mark_node_no_shards(&"unknown".into(), &index_uid, "test-source");
+        let entry = table.table.get(&key).unwrap();
+        assert_eq!(entry.nodes.get("node-1").unwrap().open_shard_count, 3);
+        assert_eq!(entry.nodes.get("node-2").unwrap().open_shard_count, 2);
+
+        // Matching incarnation: zero only the open shard count, capacity score is preserved.
+        table.mark_node_no_shards(&"node-1".into(), &index_uid, "test-source");
+        let entry = table.table.get(&key).unwrap();
+        let node_1 = entry.nodes.get("node-1").unwrap();
+        assert_eq!(node_1.open_shard_count, 0);
+        assert_eq!(node_1.capacity_score, 8);
+        // Sibling node untouched.
+        let node_2 = entry.nodes.get("node-2").unwrap();
+        assert_eq!(node_2.open_shard_count, 2);
+        assert_eq!(node_2.capacity_score, 6);
+
+        // Older incarnation argument: no-op (must not roll the entry back).
+        let stale_index_uid = IndexUid::for_test("test-index", 0);
+        table.mark_node_no_shards(&"node-2".into(), &stale_index_uid, "test-source");
+        assert_eq!(
+            table
+                .table
+                .get(&key)
+                .unwrap()
+                .nodes
+                .get("node-2")
+                .unwrap()
+                .open_shard_count,
+            2
+        );
+
+        // Newer incarnation argument: advance the entry, drop stale nodes, and force a CP
+        // re-seed (mirrors apply_capacity_update's Less arm). No node is inserted — the next
+        // CP query is responsible for repopulating the entry.
+        let newer_index_uid = IndexUid::for_test("test-index", 2);
+        table.mark_node_no_shards(&"node-2".into(), &newer_index_uid, "test-source");
+        let entry = table.table.get(&key).unwrap();
+        assert_eq!(entry.index_uid, newer_index_uid);
+        assert!(entry.nodes.is_empty());
+        assert!(!entry.seeded_from_cp);
+    }
 }