diff --git a/engine/packages/depot-client/src/database.rs b/engine/packages/depot-client/src/database.rs
index 996784b6c6..91cd2f2010 100644
--- a/engine/packages/depot-client/src/database.rs
+++ b/engine/packages/depot-client/src/database.rs
@@ -1,6 +1,8 @@
 use std::sync::Arc;
 
 use anyhow::{Result, anyhow};
+use async_trait::async_trait;
+use rivet_envoy_protocol as protocol;
 use tokio::runtime::Handle;
 
 use crate::{
@@ -23,6 +25,30 @@ pub fn vfs_name_for_actor_database(actor_id: &str, generation: u64) -> String {
 	format!("envoy-sqlite-{actor_id}-g{generation}")
 }
 
+struct GenerationFencedTransport {
+	inner: SqliteTransportHandle,
+	generation: u64,
+}
+
+#[async_trait]
+impl crate::vfs::SqliteTransport for GenerationFencedTransport {
+	async fn get_pages(
+		&self,
+		mut request: protocol::SqliteGetPagesRequest,
+	) -> Result<protocol::SqliteGetPagesResponse> {
+		request.expected_generation.get_or_insert(self.generation);
+		self.inner.get_pages(request).await
+	}
+
+	async fn commit(
+		&self,
+		mut request: protocol::SqliteCommitRequest,
+	) -> Result<protocol::SqliteCommitResponse> {
+		request.expected_generation.get_or_insert(self.generation);
+		self.inner.commit(request).await
+	}
+}
+
 pub async fn open_database_from_transport(
 	transport: SqliteTransportHandle,
 	actor_id: String,
@@ -32,6 +58,10 @@ pub async fn open_database_from_transport(
 ) -> Result<NativeDatabaseHandle> {
 	let vfs_name = vfs_name_for_actor_database(&actor_id, generation);
 	let config = VfsConfig::default();
+	let transport: SqliteTransportHandle = Arc::new(GenerationFencedTransport {
+		inner: transport,
+		generation,
+	});
 	let initial_pages = fetch_initial_pages_for_registration(transport.clone(), &actor_id, &config)
 		.await
 		.map_err(|e| anyhow!("failed to preload sqlite pages: {e}"))?;
diff --git a/engine/packages/depot-client/src/vfs.rs b/engine/packages/depot-client/src/vfs.rs
index f9ac4dcd41..e447c4d2a6 100644
--- a/engine/packages/depot-client/src/vfs.rs
+++ b/engine/packages/depot-client/src/vfs.rs
@@ -1854,6 +1854,7 @@ async fn fetch_initial_pages(
 fn is_initial_main_page_missing(message: &str) -> bool {
 	message.contains("sqlite database was not found in this bucket branch")
 		|| message.contains("sqlite meta missing for get_pages")
+		|| message == "actor does not exist"
 }
 
 fn next_temp_aux_path() -> String {
diff --git a/engine/packages/pegboard-envoy/src/ws_to_tunnel_task.rs b/engine/packages/pegboard-envoy/src/ws_to_tunnel_task.rs
index b9a33dfd80..ef161a38c8 100644
--- a/engine/packages/pegboard-envoy/src/ws_to_tunnel_task.rs
+++ b/engine/packages/pegboard-envoy/src/ws_to_tunnel_task.rs
@@ -698,7 +698,8 @@ async fn handle_sqlite_get_pages(
 	conn: &Conn,
 	request: protocol::SqliteGetPagesRequest,
 ) -> Result<protocol::SqliteGetPagesResponse> {
-	validate_sqlite_actor(ctx, conn, &request.actor_id).await?;
+	validate_sqlite_actor_for_request(ctx, conn, &request.actor_id, request.expected_generation)
+		.await?;
 
 	let actor_db = actor_db(ctx, conn, request.actor_id.clone()).await?;
 	let result = actor_db
@@ -733,7 +734,8 @@ async fn handle_sqlite_commit(
 	request: protocol::SqliteCommitRequest,
 ) -> Result<protocol::SqliteCommitResponse> {
 	let decode_request_start = Instant::now();
-	validate_sqlite_actor(ctx, conn, &request.actor_id).await?;
+	validate_sqlite_actor_for_request(ctx, conn, &request.actor_id, request.expected_generation)
+		.await?;
 	let decode_request_duration = decode_request_start.elapsed();
 	crate::metrics::SQLITE_COMMIT_ENVOY_DISPATCH_DURATION
 		.observe(decode_request_duration.as_secs_f64());
@@ -862,6 +864,19 @@ async fn validate_sqlite_actor(ctx: &StandaloneCtx, conn: &Conn, actor_id: &str)
 	Ok(())
 }
 
+async fn validate_sqlite_actor_for_request(
+	ctx: &StandaloneCtx,
+	conn: &Conn,
+	actor_id: &str,
+	expected_generation: Option<u64>,
+) -> Result<()> {
+	if let Some(generation) = expected_generation {
+		validate_remote_sqlite_generation(ctx, conn, actor_id, generation).await
+	} else {
+		validate_sqlite_actor(ctx, conn, actor_id).await
+	}
+}
+
 async fn validate_remote_sqlite_generation(
 	ctx: &StandaloneCtx,
 	conn: &Conn,
@@ -1125,11 +1140,10 @@ fn depot_error(err: &anyhow::Error) -> Option<&SqliteStorageError> {
 
 fn is_startup_database_miss(
 	err: &anyhow::Error,
-	expected_generation: Option<u64>,
+	_expected_generation: Option<u64>,
 	expected_head_txid: Option<u64>,
 ) -> bool {
-	expected_generation.is_none()
-		&& expected_head_txid.is_none()
+	expected_head_txid.is_none()
 		&& matches!(depot_error(err), Some(SqliteStorageError::DatabaseNotFound))
 }