diff --git a/src/gateway/agent-prompt.e2e.test.ts b/src/gateway/agent-prompt.e2e.test.ts
new file mode 100644
index 00000000000..80fc92e4819
--- /dev/null
+++ b/src/gateway/agent-prompt.e2e.test.ts
@@ -0,0 +1,48 @@
+import { describe, expect, it } from "vitest";
+import { buildHistoryContextFromEntries } from "../auto-reply/reply/history.js";
+import { buildAgentMessageFromConversationEntries } from "./agent-prompt.js";
+
+describe("gateway agent prompt", () => {
+  it("returns empty for no entries", () => {
+    expect(buildAgentMessageFromConversationEntries([])).toBe("");
+  });
+
+  it("returns current body when there is no history", () => {
+    expect(
+      buildAgentMessageFromConversationEntries([
+        { role: "user", entry: { sender: "User", body: "hi" } },
+      ]),
+    ).toBe("hi");
+  });
+
+  it("uses history context when there is history", () => {
+    const entries = [
+      { role: "assistant", entry: { sender: "Assistant", body: "prev" } },
+      { role: "user", entry: { sender: "User", body: "next" } },
+    ] as const;
+
+    const expected = buildHistoryContextFromEntries({
+      entries: entries.map((e) => e.entry),
+      currentMessage: "User: next",
+      formatEntry: (e) => `${e.sender}: ${e.body}`,
+    });
+
+    expect(buildAgentMessageFromConversationEntries([...entries])).toBe(expected);
+  });
+
+  it("prefers last tool entry over assistant for current message", () => {
+    const entries = [
+      { role: "user", entry: { sender: "User", body: "question" } },
+      { role: "tool", entry: { sender: "Tool:x", body: "tool output" } },
+      { role: "assistant", entry: { sender: "Assistant", body: "assistant text" } },
+    ] as const;
+
+    const expected = buildHistoryContextFromEntries({
+      entries: [entries[0].entry, entries[1].entry],
+      currentMessage: "Tool:x: tool output",
+      formatEntry: (e) => `${e.sender}: ${e.body}`,
+    });
+
+    expect(buildAgentMessageFromConversationEntries([...entries])).toBe(expected);
+  });
+});
diff --git a/src/gateway/agent-prompt.ts b/src/gateway/agent-prompt.ts
new file mode 100644
index 00000000000..58e12bacd02
--- /dev/null
+++ b/src/gateway/agent-prompt.ts
@@ -0,0 +1,43 @@
+import { buildHistoryContextFromEntries, type HistoryEntry } from "../auto-reply/reply/history.js";
+
+export type ConversationEntry = {
+  role: "user" | "assistant" | "tool";
+  entry: HistoryEntry;
+};
+
+export function buildAgentMessageFromConversationEntries(entries: ConversationEntry[]): string {
+  if (entries.length === 0) {
+    return "";
+  }
+
+  // Prefer the last user/tool entry as "current message" so the agent responds to
+  // the latest user input or tool output, not the assistant's previous message.
+  let currentIndex = -1;
+  for (let i = entries.length - 1; i >= 0; i -= 1) {
+    const role = entries[i]?.role;
+    if (role === "user" || role === "tool") {
+      currentIndex = i;
+      break;
+    }
+  }
+  if (currentIndex < 0) {
+    currentIndex = entries.length - 1;
+  }
+
+  const currentEntry = entries[currentIndex]?.entry;
+  if (!currentEntry) {
+    return "";
+  }
+
+  const historyEntries = entries.slice(0, currentIndex).map((e) => e.entry);
+  if (historyEntries.length === 0) {
+    return currentEntry.body;
+  }
+
+  const formatEntry = (entry: HistoryEntry) => `${entry.sender}: ${entry.body}`;
+  return buildHistoryContextFromEntries({
+    entries: [...historyEntries, currentEntry],
+    currentMessage: formatEntry(currentEntry),
+    formatEntry,
+  });
+}
diff --git a/src/gateway/openai-http.ts b/src/gateway/openai-http.ts
index 2b9df17cdfe..57eec192bf1 100644
--- a/src/gateway/openai-http.ts
+++ b/src/gateway/openai-http.ts
@@ -1,12 +1,15 @@
 import type { IncomingMessage, ServerResponse } from "node:http";
 import { randomUUID } from "node:crypto";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
-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";
 import { logWarn } from "../logger.js";
 import { defaultRuntime } from "../runtime.js";
+import {
+  buildAgentMessageFromConversationEntries,
+  type ConversationEntry,
+} from "./agent-prompt.js";
 import { authorizeGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
 import {
   readJsonBodyOrError,
@@ -83,8 +86,7 @@ function buildAgentPrompt(messagesUnknown: unknown): {
   const messages = asMessages(messagesUnknown);
 
   const systemParts: string[] = [];
-  const conversationEntries: Array<{ role: "user" | "assistant" | "tool"; entry: HistoryEntry }> =
-    [];
+  const conversationEntries: ConversationEntry[] = [];
 
   for (const msg of messages) {
     if (!msg || typeof msg !== "object") {
@@ -121,34 +123,7 @@ function buildAgentPrompt(messagesUnknown: unknown): {
     });
   }
 
-  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,
-        });
-      }
-    }
-  }
+  const message = buildAgentMessageFromConversationEntries(conversationEntries);
 
   return {
     message,
diff --git a/src/gateway/openresponses-http.ts b/src/gateway/openresponses-http.ts
index c4d8b9bef19..bb8cbf7e639 100644
--- a/src/gateway/openresponses-http.ts
+++ b/src/gateway/openresponses-http.ts
@@ -12,7 +12,6 @@ import type { ClientToolDefinition } from "../agents/pi-embedded-runner/run/para
 import type { ImageContent } from "../commands/agent/types.js";
 import type { GatewayHttpResponsesConfig } from "../config/types.gateway.js";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
-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";
@@ -36,6 +35,10 @@ import {
   type InputImageSource,
 } from "../media/input-files.js";
 import { defaultRuntime } from "../runtime.js";
+import {
+  buildAgentMessageFromConversationEntries,
+  type ConversationEntry,
+} from "./agent-prompt.js";
 import { authorizeGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
 import {
   readJsonBodyOrError,
@@ -196,8 +199,7 @@ export function buildAgentPrompt(input: string | ItemParam[]): {
   }
 
   const systemParts: string[] = [];
-  const conversationEntries: Array<{ role: "user" | "assistant" | "tool"; entry: HistoryEntry }> =
-    [];
+  const conversationEntries: ConversationEntry[] = [];
 
   for (const item of input) {
     if (item.type === "message") {
@@ -227,36 +229,7 @@ export function buildAgentPrompt(input: string | ItemParam[]): {
     // Skip reasoning and item_reference for prompt building (Phase 1)
   }
 
-  let message = "";
-  if (conversationEntries.length > 0) {
-    // Find the last user or tool message as the current message
-    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,
-        });
-      }
-    }
-  }
+  const message = buildAgentMessageFromConversationEntries(conversationEntries);
 
   return {
     message,