diff --git a/packages/agent/src/persistent-agent-state.test.ts b/packages/agent/src/persistent-agent-state.test.ts
new file mode 100644
index 0000000000..36e854d5c9
--- /dev/null
+++ b/packages/agent/src/persistent-agent-state.test.ts
@@ -0,0 +1,101 @@
+import {
+  lstat,
+  mkdir,
+  mkdtemp,
+  readFile,
+  readlink,
+  rm,
+  writeFile,
+} from "node:fs/promises";
+import { tmpdir } from "node:os";
+import path from "node:path";
+import { afterEach, beforeEach, describe, expect, it, vi } from "vitest";
+import { configurePersistentAgentState } from "./persistent-agent-state";
+
+describe("configurePersistentAgentState", () => {
+  let testRoot: string;
+  let homeDir: string;
+  let stateRoot: string;
+
+  beforeEach(async () => {
+    testRoot = await mkdtemp(path.join(tmpdir(), "persistent-agent-state-"));
+    homeDir = path.join(testRoot, "home");
+    stateRoot = path.join(testRoot, "workspace", ".posthog", "agent-state");
+    vi.stubEnv("CLAUDE_CONFIG_DIR", "");
+    vi.stubEnv("CODEX_HOME", "");
+  });
+
+  afterEach(async () => {
+    vi.unstubAllEnvs();
+    await rm(testRoot, { recursive: true, force: true });
+  });
+
+  it("routes native session state into the durable workspace root", async () => {
+    const claudeSkillsDir = path.join(homeDir, ".claude", "skills");
+    const claudeProjectsDir = path.join(homeDir, ".claude", "projects");
+    const claudeSessionEnvDir = path.join(homeDir, ".claude", "session-env");
+    const codexSessionsDir = path.join(homeDir, ".codex", "sessions");
+    const codexConfigPath = path.join(homeDir, ".codex", "config.toml");
+    const restoredSessionEnvDir = path.join(stateRoot, "claude", "session-env");
+    await mkdir(claudeSkillsDir, { recursive: true });
+    await mkdir(claudeProjectsDir, { recursive: true });
+    await mkdir(claudeSessionEnvDir, { recursive: true });
+    await mkdir(codexSessionsDir, { recursive: true });
+    await mkdir(path.dirname(codexConfigPath), { recursive: true });
+    await mkdir(restoredSessionEnvDir, { recursive: true });
+    await writeFile(path.join(claudeSkillsDir, "catalog.txt"), "fresh");
+    await writeFile(path.join(claudeProjectsDir, "session.jsonl"), "claude");
+    await writeFile(path.join(restoredSessionEnvDir, "restored"), "state");
+    await writeFile(path.join(codexSessionsDir, "rollout.jsonl"), "codex");
+    await writeFile(codexConfigPath, "fresh = true");
+
+    await configurePersistentAgentState(stateRoot, homeDir);
+
+    const mappings = [
+      [".claude/projects", "claude/projects"],
+      [".claude/session-env", "claude/session-env"],
+      [".claude/plans", "claude/plans"],
+      [".claude/todos", "claude/todos"],
+      [".codex/sessions", "codex/sessions"],
+      [".codex/shell_snapshots", "codex/shell_snapshots"],
+    ];
+
+    for (const [sourceRelative, targetRelative] of mappings) {
+      const source = path.join(homeDir, sourceRelative);
+      const target = path.join(stateRoot, targetRelative);
+      expect((await lstat(source)).isSymbolicLink()).toBe(true);
+      expect(path.resolve(path.dirname(source), await readlink(source))).toBe(
+        target,
+      );
+      await writeFile(path.join(source, "marker"), sourceRelative);
+      await expect(
+        readFile(path.join(target, "marker"), "utf-8"),
+      ).resolves.toBe(sourceRelative);
+    }
+
+    await configurePersistentAgentState(stateRoot, homeDir);
+
+    await expect(
+      readFile(
+        path.join(stateRoot, "claude", "projects", "session.jsonl"),
+        "utf-8",
+      ),
+    ).resolves.toBe("claude");
+    await expect(
+      readFile(
+        path.join(stateRoot, "codex", "sessions", "rollout.jsonl"),
+        "utf-8",
+      ),
+    ).resolves.toBe("codex");
+    await expect(
+      readFile(path.join(restoredSessionEnvDir, "restored"), "utf-8"),
+    ).resolves.toBe("state");
+
+    await expect(
+      readFile(path.join(claudeSkillsDir, "catalog.txt"), "utf-8"),
+    ).resolves.toBe("fresh");
+    await expect(readFile(codexConfigPath, "utf-8")).resolves.toBe(
+      "fresh = true",
+    );
+  });
+});
diff --git a/packages/agent/src/persistent-agent-state.ts b/packages/agent/src/persistent-agent-state.ts
new file mode 100644
index 0000000000..a90bfa8044
--- /dev/null
+++ b/packages/agent/src/persistent-agent-state.ts
@@ -0,0 +1,141 @@
+import {
+  cp,
+  lstat,
+  mkdir,
+  readdir,
+  readlink,
+  rename,
+  rm,
+  symlink,
+} from "node:fs/promises";
+import os from "node:os";
+import path from "node:path";
+
+interface PersistentDirectory {
+  source: string;
+  target: string;
+}
+
+function isMissingPathError(error: unknown): boolean {
+  return (
+    error instanceof Error &&
+    "code" in error &&
+    (error as NodeJS.ErrnoException).code === "ENOENT"
+  );
+}
+
+function isCrossDeviceError(error: unknown): boolean {
+  return (
+    error instanceof Error &&
+    "code" in error &&
+    (error as NodeJS.ErrnoException).code === "EXDEV"
+  );
+}
+
+async function migrateExistingDirectory(
+  source: string,
+  target: string,
+): Promise<void> {
+  const sourceEntries = await readdir(source);
+  const targetEntries = await readdir(target);
+  if (sourceEntries.length === 0) {
+    await rm(source, { recursive: true, force: true });
+    return;
+  }
+  if (targetEntries.length > 0) {
+    throw new Error(
+      `Cannot migrate persistent agent state from ${source}: ${target} is not empty`,
+    );
+  }
+
+  await rm(target, { recursive: true, force: true });
+  try {
+    await rename(source, target);
+  } catch (error) {
+    if (!isCrossDeviceError(error)) throw error;
+    await cp(source, target, {
+      recursive: true,
+      errorOnExist: true,
+      force: false,
+    });
+    await rm(source, { recursive: true, force: true });
+  }
+}
+
+async function linkPersistentDirectory({
+  source,
+  target,
+}: PersistentDirectory): Promise<void> {
+  const resolvedSource = path.resolve(source);
+  const resolvedTarget = path.resolve(target);
+  if (resolvedSource === resolvedTarget) return;
+
+  await mkdir(resolvedTarget, { recursive: true });
+  await mkdir(path.dirname(resolvedSource), { recursive: true });
+
+  try {
+    const sourceStats = await lstat(resolvedSource);
+    if (sourceStats.isSymbolicLink()) {
+      const currentTarget = path.resolve(
+        path.dirname(resolvedSource),
+        await readlink(resolvedSource),
+      );
+      if (currentTarget === resolvedTarget) return;
+      await rm(resolvedSource, { force: true });
+    } else if (sourceStats.isDirectory()) {
+      await migrateExistingDirectory(resolvedSource, resolvedTarget);
+    } else {
+      throw new Error(
+        `Persistent agent state source must be a directory: ${resolvedSource}`,
+      );
+    }
+  } catch (error) {
+    if (!isMissingPathError(error)) throw error;
+  }
+
+  await symlink(resolvedTarget, resolvedSource, "dir");
+}
+
+export async function configurePersistentAgentState(
+  stateRoot: string,
+  homeDir: string = os.homedir(),
+): Promise<void> {
+  if (!path.isAbsolute(stateRoot)) {
+    throw new Error("Persistent agent state root must be an absolute path");
+  }
+
+  const claudeConfigDir =
+    process.env.CLAUDE_CONFIG_DIR || path.join(homeDir, ".claude");
+  const codexHome = process.env.CODEX_HOME || path.join(homeDir, ".codex");
+  const directories: PersistentDirectory[] = [
+    {
+      source: path.join(claudeConfigDir, "projects"),
+      target: path.join(stateRoot, "claude", "projects"),
+    },
+    {
+      source: path.join(claudeConfigDir, "session-env"),
+      target: path.join(stateRoot, "claude", "session-env"),
+    },
+    {
+      source: path.join(claudeConfigDir, "plans"),
+      target: path.join(stateRoot, "claude", "plans"),
+    },
+    {
+      source: path.join(claudeConfigDir, "todos"),
+      target: path.join(stateRoot, "claude", "todos"),
+    },
+    {
+      source: path.join(codexHome, "sessions"),
+      target: path.join(stateRoot, "codex", "sessions"),
+    },
+    {
+      source: path.join(codexHome, "shell_snapshots"),
+      target: path.join(stateRoot, "codex", "shell_snapshots"),
+    },
+  ];
+
+  // Avoid leaving other mappings mutating after one setup operation fails.
+  for (const directory of directories) {
+    await linkPersistentDirectory(directory);
+  }
+}
diff --git a/packages/agent/src/server/agent-server.test.ts b/packages/agent/src/server/agent-server.test.ts
index 961deee65b..75dc1d2e55 100644
--- a/packages/agent/src/server/agent-server.test.ts
+++ b/packages/agent/src/server/agent-server.test.ts
@@ -1,5 +1,13 @@
 import { createHash } from "node:crypto";
-import { mkdir, mkdtemp, readFile, rm, writeFile } from "node:fs/promises";
+import {
+  lstat,
+  mkdir,
+  mkdtemp,
+  readFile,
+  readlink,
+  rm,
+  writeFile,
+} from "node:fs/promises";
 import { tmpdir } from "node:os";
 import { join } from "node:path";
 import type { ContentBlock } from "@agentclientprotocol/sdk";
@@ -441,6 +449,42 @@ describe("AgentServer HTTP Mode", () => {
         sessionInitMs: expect.any(Number),
       });
     }, 30000);
+
+    it("links native agent state before initializing the session", async () => {
+      const originalClaudeConfigDir = process.env.CLAUDE_CONFIG_DIR;
+      const originalCodexHome = process.env.CODEX_HOME;
+      const claudeConfigDir = join(repo.path, ".claude-test");
+      const codexHome = join(repo.path, ".codex-test");
+      const agentStateDir = join(repo.path, ".posthog", "agent-state");
+      process.env.CLAUDE_CONFIG_DIR = claudeConfigDir;
+      process.env.CODEX_HOME = codexHome;
+
+      try {
+        await createServer({ agentStateDir }).start();
+
+        const claudeProjects = join(claudeConfigDir, "projects");
+        const codexSessions = join(codexHome, "sessions");
+        expect((await lstat(claudeProjects)).isSymbolicLink()).toBe(true);
+        expect((await lstat(codexSessions)).isSymbolicLink()).toBe(true);
+        expect(await readlink(claudeProjects)).toBe(
+          join(agentStateDir, "claude", "projects"),
+        );
+        expect(await readlink(codexSessions)).toBe(
+          join(agentStateDir, "codex", "sessions"),
+        );
+      } finally {
+        if (originalClaudeConfigDir === undefined) {
+          delete process.env.CLAUDE_CONFIG_DIR;
+        } else {
+          process.env.CLAUDE_CONFIG_DIR = originalClaudeConfigDir;
+        }
+        if (originalCodexHome === undefined) {
+          delete process.env.CODEX_HOME;
+        } else {
+          process.env.CODEX_HOME = originalCodexHome;
+        }
+      }
+    }, 30000);
   });
 
   describe("turn completion", () => {
diff --git a/packages/agent/src/server/agent-server.ts b/packages/agent/src/server/agent-server.ts
index 75fa3d1ba3..e30a3627e0 100644
--- a/packages/agent/src/server/agent-server.ts
+++ b/packages/agent/src/server/agent-server.ts
@@ -49,6 +49,7 @@ import {
 import type { PermissionMode } from "../execution-mode";
 import { DEFAULT_CODEX_MODEL, fetchGatewayModels } from "../gateway-models";
 import { HandoffCheckpointTracker } from "../handoff-checkpoint";
+import { configurePersistentAgentState } from "../persistent-agent-state";
 import { PostHogAPIClient } from "../posthog-api";
 import {
   findPrUrls,
@@ -635,6 +636,10 @@ export class AgentServer {
   }
 
   async start(): Promise<void> {
+    if (this.config.agentStateDir) {
+      await configurePersistentAgentState(this.config.agentStateDir);
+    }
+
     await new Promise<void>((resolve) => {
       this.server = serve(
         {
diff --git a/packages/agent/src/server/bin.ts b/packages/agent/src/server/bin.ts
index 3904517b71..46828f8e47 100644
--- a/packages/agent/src/server/bin.ts
+++ b/packages/agent/src/server/bin.ts
@@ -32,6 +32,7 @@ const envSchema = z.object({
   POSTHOG_CODE_REASONING_EFFORT: z
     .enum(["low", "medium", "high", "xhigh", "max"])
     .optional(),
+  POSTHOG_AGENT_STATE_DIR: z.string().startsWith("/").optional(),
   POSTHOG_TASK_RUN_EVENT_INGEST_TOKEN: z.string().min(1).optional(),
   // Base URL for the event-ingest POST only; falls back to POSTHOG_API_URL when unset.
   POSTHOG_TASK_RUN_EVENT_INGEST_URL: z.url().optional(),
@@ -174,6 +175,7 @@ program
 
     const server = new AgentServer({
       port: parseInt(options.port, 10),
+      agentStateDir: env.POSTHOG_AGENT_STATE_DIR,
       jwtPublicKey: env.JWT_PUBLIC_KEY,
       eventIngestToken: env.POSTHOG_TASK_RUN_EVENT_INGEST_TOKEN,
       eventIngestBaseUrl: env.POSTHOG_TASK_RUN_EVENT_INGEST_URL,
diff --git a/packages/agent/src/server/types.ts b/packages/agent/src/server/types.ts
index 12465f8cb8..6bb38efba2 100644
--- a/packages/agent/src/server/types.ts
+++ b/packages/agent/src/server/types.ts
@@ -11,6 +11,7 @@ export interface ClaudeCodeConfig {
 
 export interface AgentServerConfig {
   port: number;
+  agentStateDir?: string;
   repositoryPath?: string;
   repoReadyFile?: string;
   apiUrl: string;