diff --git a/src/auto-reply/reply/agent-runner.ts b/src/auto-reply/reply/agent-runner.ts
index 62f8d7b64..eb63ce23d 100644
--- a/src/auto-reply/reply/agent-runner.ts
+++ b/src/auto-reply/reply/agent-runner.ts
@@ -19,6 +19,7 @@ import {
   updateSessionStoreEntry,
 } from "../../config/sessions.js";
 import { emitDiagnosticEvent, isDiagnosticsEnabled } from "../../infra/diagnostic-events.js";
+import { enqueueSystemEvent } from "../../infra/system-events.js";
 import { defaultRuntime } from "../../runtime.js";
 import { estimateUsageCost, resolveModelCostConfig } from "../../utils/usage-format.js";
 import { resolveResponseUsageMode, type VerboseLevel } from "../thinking.js";
@@ -36,6 +37,7 @@ import { appendUsageLine, formatResponseUsageLine } from "./agent-runner-utils.j
 import { createAudioAsVoiceBuffer, createBlockReplyPipeline } from "./block-reply-pipeline.js";
 import { resolveBlockStreamingCoalescing } from "./block-streaming.js";
 import { createFollowupRunner } from "./followup-runner.js";
+import { readPostCompactionContext } from "./post-compaction-context.js";
 import { enqueueFollowupRun, type FollowupRun, type QueueSettings } from "./queue.js";
 import { createReplyToModeFilterForChannel, resolveReplyToMode } from "./reply-threading.js";
 import { incrementRunCompactionCount, persistRunSessionUsage } from "./session-run-accounting.js";
@@ -547,6 +549,21 @@ export async function runReplyAgent(params: {
         lastCallUsage: runResult.meta.agentMeta?.lastCallUsage,
         contextTokensUsed,
       });
+
+      // Inject post-compaction workspace context for the next agent turn
+      if (sessionKey) {
+        const workspaceDir = process.cwd();
+        readPostCompactionContext(workspaceDir)
+          .then((contextContent) => {
+            if (contextContent) {
+              enqueueSystemEvent(contextContent, { sessionKey });
+            }
+          })
+          .catch(() => {
+            // Silent failure — post-compaction context is best-effort
+          });
+      }
+
       if (verboseEnabled) {
         const suffix = typeof count === "number" ? ` (count ${count})` : "";
         finalPayloads = [{ text: `🧹 Auto-compaction complete${suffix}.` }, ...finalPayloads];
diff --git a/src/auto-reply/reply/post-compaction-context.test.ts b/src/auto-reply/reply/post-compaction-context.test.ts
new file mode 100644
index 000000000..726714b33
--- /dev/null
+++ b/src/auto-reply/reply/post-compaction-context.test.ts
@@ -0,0 +1,99 @@
+import { describe, it, expect, beforeEach, afterEach } from "vitest";
+import fs from "node:fs";
+import path from "node:path";
+import { readPostCompactionContext } from "./post-compaction-context.js";
+
+describe("readPostCompactionContext", () => {
+  const tmpDir = path.join("/tmp", "test-post-compaction-" + Date.now());
+
+  beforeEach(() => {
+    fs.mkdirSync(tmpDir, { recursive: true });
+  });
+
+  afterEach(() => {
+    fs.rmSync(tmpDir, { recursive: true, force: true });
+  });
+
+  it("returns null when no AGENTS.md exists", async () => {
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).toBeNull();
+  });
+
+  it("returns null when AGENTS.md has no relevant sections", async () => {
+    fs.writeFileSync(path.join(tmpDir, "AGENTS.md"), "# My Agent\n\nSome content.\n");
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).toBeNull();
+  });
+
+  it("extracts Session Startup section", async () => {
+    const content = `# Agent Rules
+
+## Session Startup
+
+Read these files:
+1. WORKFLOW_AUTO.md
+2. memory/today.md
+
+## Other Section
+
+Not relevant.
+`;
+    fs.writeFileSync(path.join(tmpDir, "AGENTS.md"), content);
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).not.toBeNull();
+    expect(result).toContain("Session Startup");
+    expect(result).toContain("WORKFLOW_AUTO.md");
+    expect(result).toContain("Post-compaction context refresh");
+    expect(result).not.toContain("Other Section");
+  });
+
+  it("extracts Red Lines section", async () => {
+    const content = `# Rules
+
+## Red Lines
+
+Never do X.
+Never do Y.
+
+## Other
+
+Stuff.
+`;
+    fs.writeFileSync(path.join(tmpDir, "AGENTS.md"), content);
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).not.toBeNull();
+    expect(result).toContain("Red Lines");
+    expect(result).toContain("Never do X");
+  });
+
+  it("extracts both sections", async () => {
+    const content = `# Rules
+
+## Session Startup
+
+Do startup things.
+
+## Red Lines
+
+Never break things.
+
+## Other
+
+Ignore this.
+`;
+    fs.writeFileSync(path.join(tmpDir, "AGENTS.md"), content);
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).not.toBeNull();
+    expect(result).toContain("Session Startup");
+    expect(result).toContain("Red Lines");
+    expect(result).not.toContain("Other");
+  });
+
+  it("truncates when content exceeds limit", async () => {
+    const longContent = "## Session Startup\n\n" + "A".repeat(4000) + "\n\n## Other\n\nStuff.";
+    fs.writeFileSync(path.join(tmpDir, "AGENTS.md"), longContent);
+    const result = await readPostCompactionContext(tmpDir);
+    expect(result).not.toBeNull();
+    expect(result).toContain("[truncated]");
+  });
+});
diff --git a/src/auto-reply/reply/post-compaction-context.ts b/src/auto-reply/reply/post-compaction-context.ts
new file mode 100644
index 000000000..ec27a2a04
--- /dev/null
+++ b/src/auto-reply/reply/post-compaction-context.ts
@@ -0,0 +1,86 @@
+import fs from "node:fs";
+import path from "node:path";
+
+const MAX_CONTEXT_CHARS = 3000;
+
+/**
+ * Read critical sections from workspace AGENTS.md for post-compaction injection.
+ * Returns formatted system event text, or null if no AGENTS.md or no relevant sections.
+ */
+export async function readPostCompactionContext(workspaceDir: string): Promise<string | null> {
+  const agentsPath = path.join(workspaceDir, "AGENTS.md");
+
+  try {
+    if (!fs.existsSync(agentsPath)) {
+      return null;
+    }
+
+    const content = await fs.promises.readFile(agentsPath, "utf-8");
+
+    // Extract "## Session Startup" and "## Red Lines" sections
+    // Each section ends at the next "## " heading or end of file
+    const sections = extractSections(content, ["Session Startup", "Red Lines"]);
+
+    if (sections.length === 0) {
+      return null;
+    }
+
+    const combined = sections.join("\n\n");
+    const safeContent =
+      combined.length > MAX_CONTEXT_CHARS
+        ? combined.slice(0, MAX_CONTEXT_CHARS) + "\n...[truncated]..."
+        : combined;
+
+    return (
+      "[Post-compaction context refresh]\n\n" +
+      "Session was just compacted. The conversation summary above is a hint, NOT a substitute for your startup sequence. " +
+      "Execute your Session Startup sequence now — read the required files before responding to the user.\n\n" +
+      "Critical rules from AGENTS.md:\n\n" +
+      safeContent
+    );
+  } catch {
+    return null;
+  }
+}
+
+/**
+ * Extract named H2 sections from markdown content.
+ * Matches "## SectionName" and captures until the next "## " or end of string.
+ */
+function extractSections(content: string, sectionNames: string[]): string[] {
+  const results: string[] = [];
+  const lines = content.split("\n");
+
+  for (const name of sectionNames) {
+    let sectionLines: string[] = [];
+    let inSection = false;
+
+    for (const line of lines) {
+      // Check if this is the start of our target section
+      if (line.match(new RegExp(`^##\\s+${escapeRegExp(name)}\\s*$`))) {
+        inSection = true;
+        sectionLines = [line];
+        continue;
+      }
+
+      // If we're in the section, check if we've hit another H2 heading
+      if (inSection) {
+        if (line.match(/^##\s+/)) {
+          // Hit another H2 heading, stop collecting
+          break;
+        }
+        sectionLines.push(line);
+      }
+    }
+
+    if (sectionLines.length > 0) {
+      results.push(sectionLines.join("\n").trim());
+    }
+  }
+
+  return results;
+}
+
+function escapeRegExp(str: string): string {
+  return str.replace(/[.*+?^${}()|[\]\\]/g, "\\$&");
+}