diff --git a/storage_controller/src/tenant_shard.rs b/storage_controller/src/tenant_shard.rs
index 0bfca5385e..99079c57b0 100644
--- a/storage_controller/src/tenant_shard.rs
+++ b/storage_controller/src/tenant_shard.rs
@@ -1272,7 +1272,9 @@ impl TenantShard {
     }
 
     /// Return true if the optimization was really applied: it will not be applied if the optimization's
-    /// sequence is behind this tenant shard's
+    /// sequence is behind this tenant shard's or if the intent state proposed by the optimization
+    /// is not compatible with the current intent state. The later may happen when the background
+    /// reconcile loops runs concurrently with HTTP driven optimisations.
     pub(crate) fn apply_optimization(
         &mut self,
         scheduler: &mut Scheduler,
@@ -1282,6 +1284,15 @@ impl TenantShard {
             return false;
         }
 
+        if !self.validate_optimization(&optimization) {
+            tracing::info!(
+                "Skipping optimization for {} because it does not match current intent: {:?}",
+                self.tenant_shard_id,
+                optimization,
+            );
+            return false;
+        }
+
         metrics::METRICS_REGISTRY
             .metrics_group
             .storage_controller_schedule_optimization
@@ -1322,6 +1333,34 @@ impl TenantShard {
         true
     }
 
+    /// Check that the desired modifications to the intent state are compatible with
+    /// the current intent state
+    fn validate_optimization(&self, optimization: &ScheduleOptimization) -> bool {
+        match optimization.action {
+            ScheduleOptimizationAction::MigrateAttachment(MigrateAttachment {
+                old_attached_node_id,
+                new_attached_node_id,
+            }) => {
+                self.intent.attached == Some(old_attached_node_id)
+                    && self.intent.secondary.contains(&new_attached_node_id)
+            }
+            ScheduleOptimizationAction::ReplaceSecondary(ReplaceSecondary {
+                old_node_id: _,
+                new_node_id,
+            }) => {
+                // It's legal to remove a secondary that is not present in the intent state
+                !self.intent.secondary.contains(&new_node_id)
+            }
+            ScheduleOptimizationAction::CreateSecondary(new_node_id) => {
+                !self.intent.secondary.contains(&new_node_id)
+            }
+            ScheduleOptimizationAction::RemoveSecondary(_) => {
+                // It's legal to remove a secondary that is not present in the intent state
+                true
+            }
+        }
+    }
+
     /// When a shard has several secondary locations, we need to pick one in situations where
     /// we promote one of them to an attached location:
     ///  - When draining a node for restart
diff --git a/test_runner/performance/test_sharding_autosplit.py b/test_runner/performance/test_sharding_autosplit.py
index 0bb210db23..1b77831b75 100644
--- a/test_runner/performance/test_sharding_autosplit.py
+++ b/test_runner/performance/test_sharding_autosplit.py
@@ -73,6 +73,11 @@ def test_sharding_autosplit(neon_env_builder: NeonEnvBuilder, pg_bin: PgBin):
             ".*Local notification hook failed.*",
             ".*Marking shard.*for notification retry.*",
             ".*Failed to notify compute.*",
+            # As an optimization, the storage controller kicks the downloads on the secondary
+            # after the shard split. However, secondaries are created async, so it's possible
+            # that the intent state was modified, but the actual secondary hasn't been created,
+            # which results in an error.
+            ".*Error calling secondary download after shard split.*",
         ]
     )