diff --git a/packages/agent/src/server/agent-server.test.ts b/packages/agent/src/server/agent-server.test.ts
index 2b69f524c..3ba8943d7 100644
--- a/packages/agent/src/server/agent-server.test.ts
+++ b/packages/agent/src/server/agent-server.test.ts
@@ -252,6 +252,30 @@ describe("AgentServer HTTP Mode", () => {
       const body = await response.json();
       expect(body.error).toBe("No active session for this run");
     });
+
+    it("accepts structured user_message content", async () => {
+      await createServer().start();
+      const token = createToken({ run_id: "different-run-id" });
+
+      const response = await fetch(`http://localhost:${port}/command`, {
+        method: "POST",
+        headers: {
+          Authorization: `Bearer ${token}`,
+          "Content-Type": "application/json",
+        },
+        body: JSON.stringify({
+          jsonrpc: "2.0",
+          method: "user_message",
+          params: {
+            content: [{ type: "text", text: "test" }],
+          },
+        }),
+      });
+
+      expect(response.status).toBe(400);
+      const body = await response.json();
+      expect(body.error).toBe("No active session for this run");
+    });
   });
 
   describe("404 handling", () => {
diff --git a/packages/agent/src/server/agent-server.ts b/packages/agent/src/server/agent-server.ts
index 8f8fa25fe..2d14f84e0 100644
--- a/packages/agent/src/server/agent-server.ts
+++ b/packages/agent/src/server/agent-server.ts
@@ -1,3 +1,4 @@
+import type { ContentBlock } from "@agentclientprotocol/sdk";
 import {
   ClientSideConnection,
   ndJsonStream,
@@ -30,6 +31,11 @@ import type {
 import { AsyncMutex } from "../utils/async-mutex";
 import { getLlmGatewayUrl } from "../utils/gateway";
 import { Logger } from "../utils/logger";
+import {
+  deserializeCloudPrompt,
+  normalizeCloudPromptContent,
+  promptBlocksToText,
+} from "./cloud-prompt";
 import { type JwtPayload, JwtValidationError, validateJwt } from "./jwt";
 import { jsonRpcRequestSchema, validateCommandParams } from "./schemas";
 import type { AgentServerConfig } from "./types";
@@ -487,17 +493,20 @@ export class AgentServer {
     switch (method) {
       case POSTHOG_NOTIFICATIONS.USER_MESSAGE:
       case "user_message": {
-        const content = params.content as string;
+        const prompt = normalizeCloudPromptContent(
+          params.content as string | ContentBlock[],
+        );
+        const promptPreview = promptBlocksToText(prompt);
 
         this.logger.info(
-          `Processing user message (detectedPrUrl=${this.detectedPrUrl ?? "none"}): ${content.substring(0, 100)}...`,
+          `Processing user message (detectedPrUrl=${this.detectedPrUrl ?? "none"}): ${promptPreview.substring(0, 100)}...`,
         );
 
         this.session.logWriter.resetTurnMessages(this.session.payload.run_id);
 
         const result = await this.session.clientConnection.prompt({
           sessionId: this.session.acpSessionId,
-          prompt: [{ type: "text", text: content }],
+          prompt,
           ...(this.detectedPrUrl && {
             _meta: {
               prContext:
@@ -837,24 +846,33 @@ export class AgentServer {
       const initialPromptOverride = taskRun
         ? this.getInitialPromptOverride(taskRun)
         : null;
-      const initialPrompt = initialPromptOverride ?? task.description;
+      const pendingUserPrompt = this.getPendingUserPrompt(taskRun);
+      let initialPrompt: ContentBlock[] = [];
+      if (pendingUserPrompt?.length) {
+        initialPrompt = pendingUserPrompt;
+      } else if (initialPromptOverride) {
+        initialPrompt = [{ type: "text", text: initialPromptOverride }];
+      } else if (task.description) {
+        initialPrompt = [{ type: "text", text: task.description }];
+      }
 
-      if (!initialPrompt) {
+      if (initialPrompt.length === 0) {
         this.logger.warn("Task has no description, skipping initial message");
         return;
       }
 
       this.logger.info("Sending initial task message", {
         taskId: payload.task_id,
-        descriptionLength: initialPrompt.length,
+        descriptionLength: promptBlocksToText(initialPrompt).length,
         usedInitialPromptOverride: !!initialPromptOverride,
+        usedPendingUserMessage: !!pendingUserPrompt?.length,
       });
 
       this.session.logWriter.resetTurnMessages(payload.run_id);
 
       const result = await this.session.clientConnection.prompt({
         sessionId: this.session.acpSessionId,
-        prompt: [{ type: "text", text: initialPrompt }],
+        prompt: initialPrompt,
       });
 
       this.logger.info("Initial task message completed", {
@@ -886,38 +904,49 @@ export class AgentServer {
         this.resumeState.conversation,
       );
 
-      // Read the pending user message from TaskRun state (set by the workflow
+      // Read the pending user prompt from TaskRun state (set by the workflow
       // when the user sends a follow-up message that triggers a resume).
-      const pendingUserMessage = this.getPendingUserMessage(taskRun);
+      const pendingUserPrompt = this.getPendingUserPrompt(taskRun);
 
       const sandboxContext = this.resumeState.snapshotApplied
         ? `The workspace environment (all files, packages, and code changes) has been fully restored from where you left off.`
         : `The workspace files from the previous session were not restored (the file snapshot may have expired), so you are starting with a fresh environment. Your conversation history is fully preserved below.`;
 
-      let resumePrompt: string;
-      if (pendingUserMessage) {
-        // Include the pending message as the user's new question so the agent
-        // responds to it directly instead of the generic resume context.
-        resumePrompt =
-          `You are resuming a previous conversation. ${sandboxContext}\n\n` +
-          `Here is the conversation history from the previous session:\n\n` +
-          `${conversationSummary}\n\n` +
-          `The user has sent a new message:\n\n` +
-          `${pendingUserMessage}\n\n` +
-          `Respond to the user's new message above. You have full context from the previous session.`;
+      let resumePromptBlocks: ContentBlock[];
+      if (pendingUserPrompt?.length) {
+        resumePromptBlocks = [
+          {
+            type: "text",
+            text:
+              `You are resuming a previous conversation. ${sandboxContext}\n\n` +
+              `Here is the conversation history from the previous session:\n\n` +
+              `${conversationSummary}\n\n` +
+              `The user has sent a new message:\n\n`,
+          },
+          ...pendingUserPrompt,
+          {
+            type: "text",
+            text: "\n\nRespond to the user's new message above. You have full context from the previous session.",
+          },
+        ];
       } else {
-        resumePrompt =
-          `You are resuming a previous conversation. ${sandboxContext}\n\n` +
-          `Here is the conversation history from the previous session:\n\n` +
-          `${conversationSummary}\n\n` +
-          `Continue from where you left off. The user is waiting for your response.`;
+        resumePromptBlocks = [
+          {
+            type: "text",
+            text:
+              `You are resuming a previous conversation. ${sandboxContext}\n\n` +
+              `Here is the conversation history from the previous session:\n\n` +
+              `${conversationSummary}\n\n` +
+              `Continue from where you left off. The user is waiting for your response.`,
+          },
+        ];
       }
 
       this.logger.info("Sending resume message", {
         taskId: payload.task_id,
         conversationTurns: this.resumeState.conversation.length,
-        promptLength: resumePrompt.length,
-        hasPendingUserMessage: !!pendingUserMessage,
+        promptLength: promptBlocksToText(resumePromptBlocks).length,
+        hasPendingUserMessage: !!pendingUserPrompt?.length,
         snapshotApplied: this.resumeState.snapshotApplied,
       });
 
@@ -928,7 +957,7 @@ export class AgentServer {
 
       const result = await this.session.clientConnection.prompt({
         sessionId: this.session.acpSessionId,
-        prompt: [{ type: "text", text: resumePrompt }],
+        prompt: resumePromptBlocks,
       });
 
       this.logger.info("Resume message completed", {
@@ -1013,7 +1042,7 @@ export class AgentServer {
     return trimmed.length > 0 ? trimmed : null;
   }
 
-  private getPendingUserMessage(taskRun: TaskRun | null): string | null {
+  private getPendingUserPrompt(taskRun: TaskRun | null): ContentBlock[] | null {
     if (!taskRun) return null;
     const state = taskRun.state as Record<string, unknown> | undefined;
     const message = state?.pending_user_message;
@@ -1021,8 +1050,8 @@ export class AgentServer {
       return null;
     }
 
-    const trimmed = message.trim();
-    return trimmed.length > 0 ? trimmed : null;
+    const prompt = deserializeCloudPrompt(message);
+    return prompt.length > 0 ? prompt : null;
   }
 
   private getResumeRunId(taskRun: TaskRun | null): string | null {
diff --git a/packages/agent/src/server/cloud-prompt.ts b/packages/agent/src/server/cloud-prompt.ts
new file mode 100644
index 000000000..c85370dbc
--- /dev/null
+++ b/packages/agent/src/server/cloud-prompt.ts
@@ -0,0 +1,13 @@
+import type { ContentBlock } from "@agentclientprotocol/sdk";
+import { deserializeCloudPrompt, promptBlocksToText } from "@posthog/shared";
+
+export { deserializeCloudPrompt, promptBlocksToText };
+
+export function normalizeCloudPromptContent(
+  content: string | ContentBlock[],
+): ContentBlock[] {
+  if (typeof content === "string") {
+    return deserializeCloudPrompt(content);
+  }
+  return content;
+}
diff --git a/packages/agent/src/server/question-relay.test.ts b/packages/agent/src/server/question-relay.test.ts
index bdac3891f..5f73abfd3 100644
--- a/packages/agent/src/server/question-relay.test.ts
+++ b/packages/agent/src/server/question-relay.test.ts
@@ -371,6 +371,53 @@ describe("Question relay", () => {
   });
 
   describe("sendInitialTaskMessage prompt source", () => {
+    it("uses pending user prompt blocks when present", async () => {
+      vi.spyOn(server.posthogAPI, "getTask").mockResolvedValue({
+        id: "test-task-id",
+        title: "t",
+        description: "original task description",
+      } as unknown as Task);
+      vi.spyOn(server.posthogAPI, "getTaskRun").mockResolvedValue({
+        id: "test-run-id",
+        task: "test-task-id",
+        state: {
+          pending_user_message:
+            '__twig_cloud_prompt_v1__:{"blocks":[{"type":"text","text":"read this attachment"},{"type":"resource","resource":{"uri":"attachment://test.txt","text":"hello from file","mimeType":"text/plain"}}]}',
+        },
+      } as unknown as TaskRun);
+
+      const promptSpy = vi.fn().mockResolvedValue({ stopReason: "max_tokens" });
+      server.session = {
+        payload: TEST_PAYLOAD,
+        acpSessionId: "acp-session",
+        clientConnection: { prompt: promptSpy },
+        logWriter: {
+          flushAll: vi.fn().mockResolvedValue(undefined),
+          getFullAgentResponse: vi.fn().mockReturnValue(null),
+          resetTurnMessages: vi.fn(),
+          flush: vi.fn().mockResolvedValue(undefined),
+          isRegistered: vi.fn().mockReturnValue(true),
+        },
+      };
+
+      await server.sendInitialTaskMessage(TEST_PAYLOAD);
+
+      expect(promptSpy).toHaveBeenCalledWith({
+        sessionId: "acp-session",
+        prompt: [
+          { type: "text", text: "read this attachment" },
+          {
+            type: "resource",
+            resource: {
+              uri: "attachment://test.txt",
+              text: "hello from file",
+              mimeType: "text/plain",
+            },
+          },
+        ],
+      });
+    });
+
     it("uses run state initial_prompt_override when present", async () => {
       vi.spyOn(server.posthogAPI, "getTask").mockResolvedValue({
         id: "test-task-id",
diff --git a/packages/agent/src/server/schemas.test.ts b/packages/agent/src/server/schemas.test.ts
index 87b977aed..30efddc9f 100644
--- a/packages/agent/src/server/schemas.test.ts
+++ b/packages/agent/src/server/schemas.test.ts
@@ -1,5 +1,5 @@
 import { describe, expect, it } from "vitest";
-import { mcpServersSchema } from "./schemas";
+import { mcpServersSchema, validateCommandParams } from "./schemas";
 
 describe("mcpServersSchema", () => {
   it("accepts a valid HTTP server", () => {
@@ -115,3 +115,21 @@ describe("mcpServersSchema", () => {
     expect(result.success).toBe(false);
   });
 });
+
+describe("validateCommandParams", () => {
+  it("accepts structured user_message content arrays", () => {
+    const result = validateCommandParams("user_message", {
+      content: [{ type: "text", text: "hello" }],
+    });
+
+    expect(result.success).toBe(true);
+  });
+
+  it("rejects empty content array", () => {
+    const result = validateCommandParams("user_message", {
+      content: [],
+    });
+
+    expect(result.success).toBe(false);
+  });
+});
diff --git a/packages/agent/src/server/schemas.ts b/packages/agent/src/server/schemas.ts
index 7eb4348a3..2f2528759 100644
--- a/packages/agent/src/server/schemas.ts
+++ b/packages/agent/src/server/schemas.ts
@@ -42,7 +42,10 @@ export const jsonRpcRequestSchema = z.object({
 export type JsonRpcRequest = z.infer<typeof jsonRpcRequestSchema>;
 
 export const userMessageParamsSchema = z.object({
-  content: z.string().min(1, "Content is required"),
+  content: z.union([
+    z.string().min(1, "Content is required"),
+    z.array(z.record(z.string(), z.unknown())).min(1, "Content is required"),
+  ]),
 });
 
 export const commandParamsSchemas = {