diff --git a/apps/mesh/src/api/routes/decopilot/routes.ts b/apps/mesh/src/api/routes/decopilot/routes.ts
index f98229526..bb18a72f9 100644
--- a/apps/mesh/src/api/routes/decopilot/routes.ts
+++ b/apps/mesh/src/api/routes/decopilot/routes.ts
@@ -256,56 +256,14 @@ export function createDecopilotRoutes(deps: DecopilotDeps) {
 
       await saveMessagesToThread(requestMessage);
 
-      // Always create a passthrough client (all real tools) + model client.
-      // If mode is smart_tool_selection or code_execution, also create the strategy
-      // client so we get the gateway meta-tools (SEARCH/DESCRIBE/CALL_TOOL/RUN_CODE).
-      const isGatewayMode = agent.mode !== "passthrough";
-      const [modelClient, passthroughClient, strategyClient] =
-        await Promise.all([
-          clientFromConnection(modelConnection, ctx, false),
-          createVirtualClientFrom(virtualMcp, ctx, "passthrough"),
-          isGatewayMode
-            ? createVirtualClientFrom(virtualMcp, ctx, agent.mode)
-            : Promise.resolve(null),
-        ]);
-
-      closeClients = () => {
-        modelClient.close().catch(() => {});
-        passthroughClient.close().catch(() => {});
-        strategyClient?.close().catch(() => {});
-      };
-
-      // Add streaming support since agents may use streaming models
-      const streamableModelClient = withStreamingSupport(
-        modelClient,
-        models.connectionId,
-        modelConnection,
-        ctx,
-        { superUser: false },
-      );
-
-      // Extract model provider (can stay outside execute)
-      const modelProvider = await createModelProviderFromClient(
-        streamableModelClient,
-        models,
-      );
-
-      // MCP client cleanup on run abort (cancel from any pod), not request abort
+      // Register abort handler early — closeClients is populated inside
+      // execute once MCP connections are established.
       abortSignal.addEventListener("abort", () => {
         closeClients?.();
         failThread!();
       });
 
-      // Get server instructions if available (for virtual MCP agents)
-      const serverInstructions = passthroughClient.getInstructions();
-
-      // Merge platform instructions with request system messages
-      const systemPrompt = DECOPILOT_BASE_PROMPT(serverInstructions);
-      const allSystemMessages: ChatMessage[] = [
-        systemPrompt,
-        ...systemMessages,
-      ];
-
+      const isGatewayMode = agent.mode !== "passthrough";
       const maxOutputTokens =
         models.thinking.limits?.maxOutputTokens ?? DEFAULT_MAX_TOKENS;
 
@@ -313,23 +271,63 @@ export function createDecopilotRoutes(deps: DecopilotDeps) {
       let stepCount = 0;
       let pendingSave: Promise<void> | null = null;
 
+      // Pre-load conversation with a basic system prompt (no agent-specific
+      // instructions). Agent instructions come from the passthrough MCP
+      // client which is created inside execute to avoid blocking the HTTP
+      // response and triggering Cloudflare 524 timeouts.
       const allMessages = await loadAndMergeMessages(
         mem,
         requestMessage,
-        allSystemMessages,
+        [DECOPILOT_BASE_PROMPT(), ...systemMessages],
         windowSize,
       );
 
       const toolOutputMap = new Map<string, string>();
-      // 4. Create stream with writer access for data parts
-      // Pass originalMessages so handleUIMessageStreamFinish (used by onFinish)
-      // can locate tool invocations from previous assistant messages during
-      // tool-approval continuation flows.
       const uiStream = createUIMessageStream({
         originalMessages: allMessages,
         execute: async ({ writer }) => {
-          // Create tools inside execute so they have access to writer
-          // Always get the full passthrough tools (all real tools from connections)
+          // Create MCP client connections inside execute so the SSE
+          // response headers are flushed to the client before this
+          // potentially slow I/O, preventing Cloudflare 524 timeouts.
+          const [modelClient, passthroughClient, strategyClient] =
+            await Promise.all([
+              clientFromConnection(modelConnection, ctx, false),
+              createVirtualClientFrom(virtualMcp, ctx, "passthrough"),
+              isGatewayMode
+                ? createVirtualClientFrom(virtualMcp, ctx, agent.mode)
+                : Promise.resolve(null),
+            ]);
+
+          closeClients = () => {
+            modelClient.close().catch(() => {});
+            passthroughClient.close().catch(() => {});
+            strategyClient?.close().catch(() => {});
+          };
+
+          const streamableModelClient = withStreamingSupport(
+            modelClient,
+            models.connectionId,
+            modelConnection,
+            ctx,
+            { superUser: false },
+          );
+
+          const modelProvider = await createModelProviderFromClient(
+            streamableModelClient,
+            models,
+          );
+
+          // Enrich the pre-loaded messages with agent-specific instructions
+          // from the virtual MCP now that the client is available.
+          const serverInstructions = passthroughClient.getInstructions();
+          const enrichedMessages = serverInstructions?.trim()
+            ? allMessages.map((msg) =>
+                msg.id === "decopilot-system"
+                  ? DECOPILOT_BASE_PROMPT(serverInstructions)
+                  : msg,
+              )
+            : allMessages;
+
           const passthroughTools = await toolsFromMCP(
             passthroughClient,
             toolOutputMap,
@@ -337,8 +335,6 @@ export function createDecopilotRoutes(deps: DecopilotDeps) {
             toolApprovalLevel,
           );
 
-          // If using a gateway mode, also get the strategy meta-tools
-          // (GATEWAY_SEARCH_TOOLS, GATEWAY_DESCRIBE_TOOLS, GATEWAY_CALL_TOOL / GATEWAY_RUN_CODE)
           const strategyTools = strategyClient
             ? await toolsFromMCP(
                 strategyClient,
@@ -360,17 +356,12 @@ export function createDecopilotRoutes(deps: DecopilotDeps) {
             ctx,
           );
 
-          // Merge all tools: strategy meta-tools override passthrough tools with the same name,
-          // and built-in tools take final precedence.
           const tools = {
             ...passthroughTools,
             ...strategyTools,
             ...builtInTools,
           };
 
-          // In gateway modes, only expose the strategy meta-tools + built-ins to the LLM.
-          // The passthrough tools are still registered (so the AI SDK won't throw if the
-          // model calls a discovered tool directly), but the LLM won't see their schemas.
           const activeToolNames = strategyClient
             ? ([
                 ...Object.keys(strategyTools),
@@ -378,12 +369,11 @@ export function createDecopilotRoutes(deps: DecopilotDeps) {
               ] as (keyof typeof tools)[])
             : undefined;
 
-          // Process conversation with tools for validation
           const {
             systemMessages: processedSystemMessages,
             messages: processedMessages,
             originalMessages,
-          } = await processConversation(allMessages, {
+          } = await processConversation(enrichedMessages, {
             windowSize,
             models,
             tools,