diff --git a/engine/packages/pegboard-runner/src/ws_to_tunnel_task.rs b/engine/packages/pegboard-runner/src/ws_to_tunnel_task.rs
index 550e9ff216..1c4b1a7c80 100644
--- a/engine/packages/pegboard-runner/src/ws_to_tunnel_task.rs
+++ b/engine/packages/pegboard-runner/src/ws_to_tunnel_task.rs
@@ -860,6 +860,9 @@ async fn handle_tunnel_message_mk2(
 	authorized_tunnel_routes: &HashMap<(protocol::mk2::GatewayId, protocol::mk2::RequestId), ()>,
 	msg: protocol::mk2::ToServerTunnelMessage,
 ) -> Result<()> {
+	let route = (msg.message_id.gateway_id, msg.message_id.request_id);
+	let clear_route = should_clear_tunnel_route_mk2(&msg.message_kind);
+
 	// Extract inner data length before consuming msg
 	let inner_data_len = tunnel_message_inner_data_len_mk2(&msg.message_kind);
 
@@ -868,10 +871,7 @@ async fn handle_tunnel_message_mk2(
 		return Err(errors::WsError::InvalidPacket("payload too large".to_string()).build());
 	}
 
-	if !authorized_tunnel_routes
-		.contains_async(&(msg.message_id.gateway_id, msg.message_id.request_id))
-		.await
-	{
+	if !authorized_tunnel_routes.contains_async(&route).await {
 		return Err(
 			errors::WsError::InvalidPacket("unauthorized tunnel message".to_string()).build(),
 		);
@@ -899,6 +899,10 @@ async fn handle_tunnel_message_mk2(
 			)
 		})?;
 
+	if clear_route {
+		authorized_tunnel_routes.remove_async(&route).await;
+	}
+
 	Ok(())
 }
 
@@ -909,6 +913,9 @@ async fn handle_tunnel_message_mk1(
 	authorized_tunnel_routes: &HashMap<(protocol::mk2::GatewayId, protocol::mk2::RequestId), ()>,
 	msg: protocol::ToServerTunnelMessage,
 ) -> Result<()> {
+	let route = (msg.message_id.gateway_id, msg.message_id.request_id);
+	let clear_route = should_clear_tunnel_route_mk1(&msg.message_kind);
+
 	// Ignore DeprecatedTunnelAck messages (used only for backwards compatibility)
 	if matches!(
 		msg.message_kind,
@@ -925,10 +932,7 @@ async fn handle_tunnel_message_mk1(
 		return Err(errors::WsError::InvalidPacket("payload too large".to_string()).build());
 	}
 
-	if !authorized_tunnel_routes
-		.contains_async(&(msg.message_id.gateway_id, msg.message_id.request_id))
-		.await
-	{
+	if !authorized_tunnel_routes.contains_async(&route).await {
 		return Err(
 			errors::WsError::InvalidPacket("unauthorized tunnel message".to_string()).build(),
 		);
@@ -950,9 +954,35 @@ async fn handle_tunnel_message_mk1(
 			)
 		})?;
 
+	if clear_route {
+		authorized_tunnel_routes.remove_async(&route).await;
+	}
+
 	Ok(())
 }
 
+fn should_clear_tunnel_route_mk2(msg_kind: &protocol::mk2::ToServerTunnelMessageKind) -> bool {
+	match msg_kind {
+		protocol::mk2::ToServerTunnelMessageKind::ToServerResponseStart(response) => {
+			!response.stream
+		}
+		protocol::mk2::ToServerTunnelMessageKind::ToServerResponseChunk(chunk) => chunk.finish,
+		protocol::mk2::ToServerTunnelMessageKind::ToServerResponseAbort
+		| protocol::mk2::ToServerTunnelMessageKind::ToServerWebSocketClose(_) => true,
+		_ => false,
+	}
+}
+
+fn should_clear_tunnel_route_mk1(msg_kind: &protocol::ToServerTunnelMessageKind) -> bool {
+	match msg_kind {
+		protocol::ToServerTunnelMessageKind::ToServerResponseStart(response) => !response.stream,
+		protocol::ToServerTunnelMessageKind::ToServerResponseChunk(chunk) => chunk.finish,
+		protocol::ToServerTunnelMessageKind::ToServerResponseAbort
+		| protocol::ToServerTunnelMessageKind::ToServerWebSocketClose(_) => true,
+		_ => false,
+	}
+}
+
 /// Returns the length of the inner data payload for a tunnel message kind.
 fn tunnel_message_inner_data_len_mk2(kind: &protocol::mk2::ToServerTunnelMessageKind) -> usize {
 	use protocol::mk2::ToServerTunnelMessageKind;
diff --git a/engine/packages/pegboard-runner/tests/support/ws_to_tunnel_task.rs b/engine/packages/pegboard-runner/tests/support/ws_to_tunnel_task.rs
index 53b4278136..fbfcf2dc66 100644
--- a/engine/packages/pegboard-runner/tests/support/ws_to_tunnel_task.rs
+++ b/engine/packages/pegboard-runner/tests/support/ws_to_tunnel_task.rs
@@ -25,6 +25,74 @@ fn response_abort_message_mk2(
 	}
 }
 
+fn response_start_message_mk2(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+) -> protocol::mk2::ToServerTunnelMessage {
+	response_start_message_mk2_with_stream(gateway_id, request_id, false)
+}
+
+fn response_start_message_mk2_with_stream(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+	stream: bool,
+) -> protocol::mk2::ToServerTunnelMessage {
+	protocol::mk2::ToServerTunnelMessage {
+		message_id: protocol::mk2::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::mk2::ToServerTunnelMessageKind::ToServerResponseStart(
+			protocol::mk2::ToServerResponseStart {
+				status: 200,
+				headers: Default::default(),
+				body: None,
+				stream,
+			},
+		),
+	}
+}
+
+fn response_chunk_message_mk2(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+	finish: bool,
+) -> protocol::mk2::ToServerTunnelMessage {
+	protocol::mk2::ToServerTunnelMessage {
+		message_id: protocol::mk2::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::mk2::ToServerTunnelMessageKind::ToServerResponseChunk(
+			protocol::mk2::ToServerResponseChunk {
+				body: b"chunk".to_vec(),
+				finish,
+			},
+		),
+	}
+}
+
+fn websocket_message_mk2(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+) -> protocol::mk2::ToServerTunnelMessage {
+	protocol::mk2::ToServerTunnelMessage {
+		message_id: protocol::mk2::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::mk2::ToServerTunnelMessageKind::ToServerWebSocketMessage(
+			protocol::mk2::ToServerWebSocketMessage {
+				data: b"ping".to_vec(),
+				binary: false,
+			},
+		),
+	}
+}
+
 fn response_abort_message_mk1(
 	gateway_id: protocol::mk2::GatewayId,
 	request_id: protocol::mk2::RequestId,
@@ -39,6 +107,74 @@ fn response_abort_message_mk1(
 	}
 }
 
+fn websocket_message_mk1(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+) -> protocol::ToServerTunnelMessage {
+	protocol::ToServerTunnelMessage {
+		message_id: protocol::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::ToServerTunnelMessageKind::ToServerWebSocketMessage(
+			protocol::ToServerWebSocketMessage {
+				data: b"ping".to_vec(),
+				binary: false,
+			},
+		),
+	}
+}
+
+fn response_start_message_mk1(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+) -> protocol::ToServerTunnelMessage {
+	response_start_message_mk1_with_stream(gateway_id, request_id, false)
+}
+
+fn response_start_message_mk1_with_stream(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+	stream: bool,
+) -> protocol::ToServerTunnelMessage {
+	protocol::ToServerTunnelMessage {
+		message_id: protocol::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::ToServerTunnelMessageKind::ToServerResponseStart(
+			protocol::ToServerResponseStart {
+				status: 200,
+				headers: Default::default(),
+				body: None,
+				stream,
+			},
+		),
+	}
+}
+
+fn response_chunk_message_mk1(
+	gateway_id: protocol::mk2::GatewayId,
+	request_id: protocol::mk2::RequestId,
+	finish: bool,
+) -> protocol::ToServerTunnelMessage {
+	protocol::ToServerTunnelMessage {
+		message_id: protocol::MessageId {
+			gateway_id,
+			request_id,
+			message_index: 0,
+		},
+		message_kind: protocol::ToServerTunnelMessageKind::ToServerResponseChunk(
+			protocol::ToServerResponseChunk {
+				body: b"chunk".to_vec(),
+				finish,
+			},
+		),
+	}
+}
+
 #[tokio::test]
 async fn rejects_unissued_mk2_tunnel_message_pairs() {
 	let pubsub = memory_pubsub("pegboard-runner-ws-to-tunnel-test-reject-mk2");
@@ -82,7 +218,7 @@ async fn republishes_issued_mk2_tunnel_message_pairs() {
 		&pubsub,
 		1024,
 		&authorized_tunnel_routes,
-		response_abort_message_mk2(gateway_id, request_id),
+		websocket_message_mk2(gateway_id, request_id),
 	)
 	.await
 	.unwrap();
@@ -92,6 +228,11 @@ async fn republishes_issued_mk2_tunnel_message_pairs() {
 		.unwrap()
 		.unwrap();
 	assert!(matches!(msg, NextOutput::Message(_)));
+	assert!(
+		authorized_tunnel_routes
+			.contains_async(&(gateway_id, request_id))
+			.await
+	);
 }
 
 #[tokio::test]
@@ -137,7 +278,7 @@ async fn republishes_issued_mk1_tunnel_message_pairs() {
 		&pubsub,
 		1024,
 		&authorized_tunnel_routes,
-		response_abort_message_mk1(gateway_id, request_id),
+		websocket_message_mk1(gateway_id, request_id),
 	)
 	.await
 	.unwrap();
@@ -147,4 +288,9 @@ async fn republishes_issued_mk1_tunnel_message_pairs() {
 		.unwrap()
 		.unwrap();
 	assert!(matches!(msg, NextOutput::Message(_)));
+	assert!(
+		authorized_tunnel_routes
+			.contains_async(&(gateway_id, request_id))
+			.await
+	);
 }