diff --git a/storage_controller/src/http.rs b/storage_controller/src/http.rs
index 46b6f4f2bf..afefe8598c 100644
--- a/storage_controller/src/http.rs
+++ b/storage_controller/src/http.rs
@@ -381,14 +381,16 @@ async fn handle_tenant_timeline_delete(
         R: std::future::Future<Output = Result<StatusCode, ApiError>> + Send + 'static,
         F: Fn(Arc<Service>) -> R + Send + Sync + 'static,
     {
+        // On subsequent retries, wait longer.
+        // Enable callers with a 25 second request timeout to reliably get a response
+        const MAX_WAIT: Duration = Duration::from_secs(25);
+        const MAX_RETRY_PERIOD: Duration = Duration::from_secs(5);
+
         let started_at = Instant::now();
+
         // To keep deletion reasonably snappy for small tenants, initially check after 1 second if deletion
         // completed.
         let mut retry_period = Duration::from_secs(1);
-        // On subsequent retries, wait longer.
-        let max_retry_period = Duration::from_secs(5);
-        // Enable callers with a 30 second request timeout to reliably get a response
-        let max_wait = Duration::from_secs(25);
 
         loop {
             let status = f(service.clone()).await?;
@@ -396,7 +398,11 @@ async fn handle_tenant_timeline_delete(
                 StatusCode::ACCEPTED => {
                     tracing::info!("Deletion accepted, waiting to try again...");
                     tokio::time::sleep(retry_period).await;
-                    retry_period = max_retry_period;
+                    retry_period = MAX_RETRY_PERIOD;
+                }
+                StatusCode::CONFLICT => {
+                    tracing::info!("Deletion already in progress, waiting to try again...");
+                    tokio::time::sleep(retry_period).await;
                 }
                 StatusCode::NOT_FOUND => {
                     tracing::info!("Deletion complete");
@@ -409,7 +415,7 @@ async fn handle_tenant_timeline_delete(
             }
 
             let now = Instant::now();
-            if now + retry_period > started_at + max_wait {
+            if now + retry_period > started_at + MAX_WAIT {
                 tracing::info!("Deletion timed out waiting for 404");
                 // REQUEST_TIMEOUT would be more appropriate, but CONFLICT is already part of
                 // the pageserver's swagger definition for this endpoint, and has the same desired
diff --git a/storage_controller/src/service.rs b/storage_controller/src/service.rs
index ab2c3b5e48..01aa8f1dab 100644
--- a/storage_controller/src/service.rs
+++ b/storage_controller/src/service.rs
@@ -3630,14 +3630,21 @@ impl Service {
                 );
 
                 let client = PageserverClient::new(node.get_id(), node.base_url(), jwt.as_deref());
-                client
+                let res = client
                     .timeline_delete(tenant_shard_id, timeline_id)
-                    .await
-                    .map_err(|e| {
-                        ApiError::InternalServerError(anyhow::anyhow!(
-                            "Error deleting timeline {timeline_id} on {tenant_shard_id} on node {node}: {e}",
-                        ))
-                    })
+                    .await;
+
+                match res {
+                    Ok(ok) => Ok(ok),
+                    Err(mgmt_api::Error::ApiError(StatusCode::CONFLICT, _)) => Ok(StatusCode::CONFLICT),
+                    Err(e) => {
+                        Err(
+                            ApiError::InternalServerError(anyhow::anyhow!(
+                                "Error deleting timeline {timeline_id} on {tenant_shard_id} on node {node}: {e}",
+                            ))
+                        )
+                    }
+                }
             }
 
             let locations = targets.0.iter().map(|t| (*t.0, t.1.latest.node.clone())).collect();
@@ -3652,7 +3659,13 @@ impl Service {
                 })
                 .await?;
 
-            // If any shards >0 haven't finished deletion yet, don't start deletion on shard zero
+            // If any shards >0 haven't finished deletion yet, don't start deletion on shard zero.
+            // We return 409 (Conflict) if deletion was already in progress on any of the shards
+            // and 202 (Accepted) if deletion was not already in progress on any of the shards.
+            if statuses.iter().any(|s| s == &StatusCode::CONFLICT) {
+                return Ok(StatusCode::CONFLICT);
+            }
+
             if statuses.iter().any(|s| s != &StatusCode::NOT_FOUND) {
                 return Ok(StatusCode::ACCEPTED);
             }