diff --git a/extensions/cli/src/commands/devbox-entrypoint.md b/extensions/cli/src/commands/devbox-entrypoint.md
new file mode 100644
index 000000000..bd4382058
--- /dev/null
+++ b/extensions/cli/src/commands/devbox-entrypoint.md
@@ -0,0 +1,12 @@
+# Devbox entrypoint behavior (cn serve)
+
+Context: runloop resumes a devbox by re-running the same entrypoint script, which invokes `cn serve --id <agentId> ...`. Because the entrypoint always replays, the CLI must avoid duplicating state on restart.
+
+- **Session reuse:** `serve` now calls `loadOrCreateSessionById` when `--id` is provided so the same session file is reused instead of generating a new UUID. This keeps chat history intact across suspend/resume.
+- **Skip replaying the initial prompt:** `shouldQueueInitialPrompt` checks existing history and only queues the initial prompt when there are no non-system messages. This prevents the first prompt from being resent when a suspended devbox restarts.
+- **Environment persistence:** The devbox entrypoint (control-plane) writes all env vars to `~/.continue/devbox-env` and sources it before `cn serve`, so keys survive suspend/resume. The CLI assumes env is already present.
+
+Operational notes:
+
+- Changing the entrypoint is expensive; prefer adapting CLI/session behavior as above.
+- When testing suspend/resume, confirm a single session file under `~/.continue/sessions` for the agent id and that follow-up messages append normally without replaying the first prompt.
diff --git a/extensions/cli/src/commands/serve.initialPrompt.test.ts b/extensions/cli/src/commands/serve.initialPrompt.test.ts
new file mode 100644
index 000000000..6e11b4571
--- /dev/null
+++ b/extensions/cli/src/commands/serve.initialPrompt.test.ts
@@ -0,0 +1,30 @@
+import type { ChatHistoryItem } from "core/index.js";
+import { describe, expect, it } from "vitest";
+
+import { shouldQueueInitialPrompt } from "./serve.js";
+
+const systemOnly: ChatHistoryItem[] = [
+  { message: { role: "system", content: "sys" }, contextItems: [] },
+];
+
+const withConversation: ChatHistoryItem[] = [
+  ...systemOnly,
+  { message: { role: "user", content: "hi" }, contextItems: [] },
+  { message: { role: "assistant", content: "hello" }, contextItems: [] },
+];
+
+describe("shouldQueueInitialPrompt", () => {
+  it("returns false when no prompt is provided", () => {
+    expect(shouldQueueInitialPrompt([], undefined)).toBe(false);
+    expect(shouldQueueInitialPrompt([], null)).toBe(false);
+  });
+
+  it("returns true when prompt exists and only system history is present", () => {
+    expect(shouldQueueInitialPrompt([], "prompt")).toBe(true);
+    expect(shouldQueueInitialPrompt(systemOnly, "prompt")).toBe(true);
+  });
+
+  it("returns false when prompt exists but conversation already has non-system messages", () => {
+    expect(shouldQueueInitialPrompt(withConversation, "prompt")).toBe(false);
+  });
+});
diff --git a/extensions/cli/src/commands/serve.ts b/extensions/cli/src/commands/serve.ts
index 8eb6ef1e9..f77e86f41 100644
--- a/extensions/cli/src/commands/serve.ts
+++ b/extensions/cli/src/commands/serve.ts
@@ -51,6 +51,26 @@ interface ServeOptions extends ExtendedCommandOptions {
   id?: string;
 }
 
+/**
+ * Decide whether to enqueue the initial prompt on server startup.
+ * We only want to send it when starting a brand-new session; if any non-system
+ * messages already exist (e.g., after resume), skip to avoid replaying.
+ */
+export function shouldQueueInitialPrompt(
+  history: ChatHistoryItem[],
+  prompt?: string | null,
+): boolean {
+  if (!prompt) {
+    return false;
+  }
+
+  // If there are any non-system messages, we already have conversation context
+  const hasConversation = history.some(
+    (item) => item.message.role !== "system",
+  );
+  return !hasConversation;
+}
+
 // eslint-disable-next-line max-statements
 export async function serve(prompt?: string, options: ServeOptions = {}) {
   await posthogService.capture("sessionStart", {});
@@ -419,10 +439,28 @@ export async function serve(prompt?: string, options: ServeOptions = {}) {
       agentFileState?.agentFile?.prompt,
       actualPrompt,
     );
+
     if (initialPrompt) {
-      console.log(chalk.dim("\nProcessing initial prompt..."));
-      await messageQueue.enqueueMessage(initialPrompt);
-      processMessages(state, llmApi);
+      const existingHistory =
+        (() => {
+          try {
+            return services.chatHistory.getHistory();
+          } catch {
+            return state.session.history;
+          }
+        })() ?? [];
+
+      if (shouldQueueInitialPrompt(existingHistory, initialPrompt)) {
+        logger.info(chalk.dim("\nProcessing initial prompt..."));
+        await messageQueue.enqueueMessage(initialPrompt);
+        processMessages(state, llmApi);
+      } else {
+        logger.info(
+          chalk.dim(
+            "Skipping initial prompt because existing conversation history was found.",
+          ),
+        );
+      }
     }
   });