diff --git a/src/agents/embedded-agent-runner.limithistoryturns.test.ts b/src/agents/embedded-agent-runner.limithistoryturns.test.ts
index daede5f422b..5d3df657c6b 100644
--- a/src/agents/embedded-agent-runner.limithistoryturns.test.ts
+++ b/src/agents/embedded-agent-runner.limithistoryturns.test.ts
@@ -118,6 +118,50 @@ describe("limitHistoryTurns", () => {
     expect(limited[1].role).toBe("assistant");
   });
 
+  it("preserves leading compactionSummary when limiting", () => {
+    const compactionSummary: AgentMessage = {
+      role: "compactionSummary",
+      summary: "Previous conversation about topic X",
+      tokensBefore: 5000,
+      tokensAfter: 2000,
+      timestamp: Date.now(),
+    } as AgentMessage;
+    const messages = [
+      compactionSummary,
+      ...makeMessages(["user", "assistant", "user", "assistant"]),
+    ];
+    const limited = limitHistoryTurns(messages, 1);
+    // compactionSummary is preserved, last 1 user turn + assistant kept
+    expect(limited.length).toBe(3);
+    expect(limited[0].role).toBe("compactionSummary");
+    expect(firstText(limited[1])).toBe("message 2");
+  });
+
+  it("preserves leading branchSummary when limiting", () => {
+    const branchSummary: AgentMessage = {
+      role: "branchSummary",
+      summary: "Branch context",
+      fromId: "abc",
+      timestamp: Date.now(),
+    } as AgentMessage;
+    const messages = [branchSummary, ...makeMessages(["user", "assistant", "user", "assistant"])];
+    const limited = limitHistoryTurns(messages, 1);
+    expect(limited.length).toBe(3);
+    expect(limited[0].role).toBe("branchSummary");
+  });
+
+  it("returns all when only non-conversation messages exist", () => {
+    const compactionSummary: AgentMessage = {
+      role: "compactionSummary",
+      summary: "Summary only",
+      tokensBefore: 1000,
+      timestamp: Date.now(),
+    } as AgentMessage;
+    const limited = limitHistoryTurns([compactionSummary], 2);
+    expect(limited).toHaveLength(1);
+    expect(limited[0].role).toBe("compactionSummary");
+  });
+
   it("preserves message content integrity", () => {
     // Limiting should slice whole turns, not mutate tool calls or message bodies.
     const messages: AgentMessage[] = [
diff --git a/src/agents/embedded-agent-runner/history.ts b/src/agents/embedded-agent-runner/history.ts
index 936e833d6a2..59b53317a4c 100644
--- a/src/agents/embedded-agent-runner/history.ts
+++ b/src/agents/embedded-agent-runner/history.ts
@@ -16,6 +16,10 @@ function stripThreadSuffix(value: string): string {
 /**
  * Limits conversation history to the last N user turns (and their associated
  * assistant responses). This reduces token usage for long-running DM sessions.
+ *
+ * Leading non-conversation messages (e.g. compactionSummary, branchSummary)
+ * placed at index 0 by buildSessionContext are always preserved, since they
+ * carry summarized pre-compaction context that history limiting must not drop.
  */
 export function limitHistoryTurns(
   messages: AgentMessage[],
@@ -25,14 +29,30 @@ export function limitHistoryTurns(
     return messages;
   }
 
-  let userCount = 0;
-  let lastUserIndex = messages.length;
+  // Preserve leading non-conversation messages (compactionSummary, branchSummary, etc.)
+  // that buildSessionContext places at index 0 to carry pre-compaction context.
+  let conversationStart = 0;
+  while (conversationStart < messages.length) {
+    const role = messages[conversationStart].role;
+    if (role === "user" || role === "assistant") {
+      break;
+    }
+    conversationStart++;
+  }
 
-  for (let i = messages.length - 1; i >= 0; i--) {
-    if (messages[i].role === "user") {
+  const tail = messages.slice(conversationStart);
+  if (tail.length === 0) {
+    return messages;
+  }
+
+  let userCount = 0;
+  let lastUserIndex = tail.length;
+
+  for (let i = tail.length - 1; i >= 0; i--) {
+    if (tail[i].role === "user") {
       userCount++;
       if (userCount > limit) {
-        return messages.slice(lastUserIndex);
+        return [...messages.slice(0, conversationStart), ...tail.slice(lastUserIndex)];
       }
       lastUserIndex = i;
     }