diff --git a/src/gateway/openai-http.e2e.test.ts b/src/gateway/openai-http.e2e.test.ts
index f44b18dce..08dc11bbc 100644
--- a/src/gateway/openai-http.e2e.test.ts
+++ b/src/gateway/openai-http.e2e.test.ts
@@ -1,5 +1,7 @@
 import { describe, expect, it } from "vitest";
 
+import { HISTORY_CONTEXT_MARKER } from "../auto-reply/reply/history.js";
+import { CURRENT_MESSAGE_MARKER } from "../auto-reply/reply/mentions.js";
 import { emitAgentEvent } from "../infra/agent-events.js";
 import { agentCommand, getFreePort, installGatewayTestHooks } from "./test-helpers.js";
 
@@ -262,6 +264,121 @@ describe("OpenAI-compatible HTTP API (e2e)", () => {
     }
   });
 
+  it("includes conversation history when multiple messages are provided", async () => {
+    agentCommand.mockResolvedValueOnce({
+      payloads: [{ text: "I am Claude" }],
+    } as never);
+
+    const port = await getFreePort();
+    const server = await startServer(port);
+    try {
+      const res = await postChatCompletions(port, {
+        model: "clawdbot",
+        messages: [
+          { role: "system", content: "You are a helpful assistant." },
+          { role: "user", content: "Hello, who are you?" },
+          { role: "assistant", content: "I am Claude." },
+          { role: "user", content: "What did I just ask you?" },
+        ],
+      });
+      expect(res.status).toBe(200);
+
+      const [opts] = agentCommand.mock.calls[0] ?? [];
+      const message = (opts as { message?: string } | undefined)?.message ?? "";
+      expect(message).toContain(HISTORY_CONTEXT_MARKER);
+      expect(message).toContain("User: Hello, who are you?");
+      expect(message).toContain("Assistant: I am Claude.");
+      expect(message).toContain(CURRENT_MESSAGE_MARKER);
+      expect(message).toContain("User: What did I just ask you?");
+    } finally {
+      await server.close({ reason: "test done" });
+    }
+  });
+
+  it("does not include history markers for single message", async () => {
+    agentCommand.mockResolvedValueOnce({
+      payloads: [{ text: "hello" }],
+    } as never);
+
+    const port = await getFreePort();
+    const server = await startServer(port);
+    try {
+      const res = await postChatCompletions(port, {
+        model: "clawdbot",
+        messages: [
+          { role: "system", content: "You are a helpful assistant." },
+          { role: "user", content: "Hello" },
+        ],
+      });
+      expect(res.status).toBe(200);
+
+      const [opts] = agentCommand.mock.calls[0] ?? [];
+      const message = (opts as { message?: string } | undefined)?.message ?? "";
+      expect(message).not.toContain(HISTORY_CONTEXT_MARKER);
+      expect(message).not.toContain(CURRENT_MESSAGE_MARKER);
+      expect(message).toBe("Hello");
+    } finally {
+      await server.close({ reason: "test done" });
+    }
+  });
+
+  it("treats developer role same as system role", async () => {
+    agentCommand.mockResolvedValueOnce({
+      payloads: [{ text: "hello" }],
+    } as never);
+
+    const port = await getFreePort();
+    const server = await startServer(port);
+    try {
+      const res = await postChatCompletions(port, {
+        model: "clawdbot",
+        messages: [
+          { role: "developer", content: "You are a helpful assistant." },
+          { role: "user", content: "Hello" },
+        ],
+      });
+      expect(res.status).toBe(200);
+
+      const [opts] = agentCommand.mock.calls[0] ?? [];
+      const extraSystemPrompt = (opts as { extraSystemPrompt?: string } | undefined)
+        ?.extraSystemPrompt ?? "";
+      expect(extraSystemPrompt).toBe("You are a helpful assistant.");
+    } finally {
+      await server.close({ reason: "test done" });
+    }
+  });
+
+  it("includes tool output when it is the latest message", async () => {
+    agentCommand.mockResolvedValueOnce({
+      payloads: [{ text: "ok" }],
+    } as never);
+
+    const port = await getFreePort();
+    const server = await startServer(port);
+    try {
+      const res = await postChatCompletions(port, {
+        model: "clawdbot",
+        messages: [
+          { role: "system", content: "You are a helpful assistant." },
+          { role: "user", content: "What's the weather?" },
+          { role: "assistant", content: "Checking the weather." },
+          { role: "tool", content: "Sunny, 70F." },
+        ],
+      });
+      expect(res.status).toBe(200);
+
+      const [opts] = agentCommand.mock.calls[0] ?? [];
+      const message = (opts as { message?: string } | undefined)?.message ?? "";
+      expect(message).toContain(HISTORY_CONTEXT_MARKER);
+      expect(message).toContain("User: What's the weather?");
+      expect(message).toContain("Assistant: Checking the weather.");
+      expect(message).toContain(CURRENT_MESSAGE_MARKER);
+      expect(message).toContain("Tool: Sunny, 70F.");
+    } finally {
+      await server.close({ reason: "test done" });
+    }
+  });
+
   it("returns a non-streaming OpenAI chat.completion response", async () => {
     agentCommand.mockResolvedValueOnce({
       payloads: [{ text: "hello" }],
diff --git a/src/gateway/openai-http.ts b/src/gateway/openai-http.ts
index 5b475f4af..64709c4df 100644
--- a/src/gateway/openai-http.ts
+++ b/src/gateway/openai-http.ts
@@ -1,6 +1,7 @@
 import { randomUUID } from "node:crypto";
 import type { IncomingMessage, ServerResponse } from "node:http";
 
+import { buildHistoryContextFromEntries, type HistoryEntry } from "../auto-reply/reply/history.js";
 import { createDefaultDeps } from "../cli/deps.js";
 import { agentCommand } from "../commands/agent.js";
 import { emitAgentEvent, onAgentEvent } from "../infra/agent-events.js";
@@ -17,6 +18,7 @@ type OpenAiHttpOptions = {
 type OpenAiChatMessage = {
   role?: unknown;
   content?: unknown;
+  name?: unknown;
 };
 
 type OpenAiChatCompletionRequest = {
@@ -85,24 +87,69 @@ function buildAgentPrompt(messagesUnknown: unknown): {
   const messages = asMessages(messagesUnknown);
 
   const systemParts: string[] = [];
-  let lastUser = "";
+  const conversationEntries: Array<{ role: "user" | "assistant" | "tool"; entry: HistoryEntry }> =
+    [];
 
   for (const msg of messages) {
     if (!msg || typeof msg !== "object") continue;
     const role = typeof msg.role === "string" ? msg.role.trim() : "";
     const content = extractTextContent(msg.content).trim();
     if (!role || !content) continue;
-    if (role === "system") {
+    if (role === "system" || role === "developer") {
       systemParts.push(content);
       continue;
     }
-    if (role === "user") {
-      lastUser = content;
+
+    const normalizedRole = role === "function" ? "tool" : role;
+    if (normalizedRole !== "user" && normalizedRole !== "assistant" && normalizedRole !== "tool") {
+      continue;
+    }
+
+    const name = typeof msg.name === "string" ? msg.name.trim() : "";
+    const sender =
+      normalizedRole === "assistant"
+        ? "Assistant"
+        : normalizedRole === "user"
+          ? "User"
+          : name
+            ? `Tool:${name}`
+            : "Tool";
+
+    conversationEntries.push({
+      role: normalizedRole,
+      entry: { sender, body: content },
+    });
+  }
+
+  let message = "";
+  if (conversationEntries.length > 0) {
+    let currentIndex = -1;
+    for (let i = conversationEntries.length - 1; i >= 0; i -= 1) {
+      const entryRole = conversationEntries[i]?.role;
+      if (entryRole === "user" || entryRole === "tool") {
+        currentIndex = i;
+        break;
+      }
+    }
+    if (currentIndex < 0) currentIndex = conversationEntries.length - 1;
+    const currentEntry = conversationEntries[currentIndex]?.entry;
+    if (currentEntry) {
+      const historyEntries = conversationEntries.slice(0, currentIndex).map((entry) => entry.entry);
+      if (historyEntries.length === 0) {
+        message = currentEntry.body;
+      } else {
+        const formatEntry = (entry: HistoryEntry) => `${entry.sender}: ${entry.body}`;
+        message = buildHistoryContextFromEntries({
+          entries: [...historyEntries, currentEntry],
+          currentMessage: formatEntry(currentEntry),
+          formatEntry,
+        });
+      }
     }
   }
 
   return {
-    message: lastUser,
+    message,
     extraSystemPrompt: systemParts.length > 0 ? systemParts.join("\n\n") : undefined,
   };
 }