diff --git a/src/workspace-store.ts b/src/workspace-store.ts
index 39c2ed09..6e0a5b68 100644
--- a/src/workspace-store.ts
+++ b/src/workspace-store.ts
@@ -1,4 +1,4 @@
-import { eq } from "drizzle-orm";
+import { desc, eq } from "drizzle-orm";
 import { openDatabase, type DatabaseHandle } from "./db/client.js";
 import {
   workspaceSessions,
@@ -31,6 +31,7 @@ export interface WorkspaceStore {
     managed?: boolean;
   }): WorkspaceSession;
   getSession(id: string): WorkspaceSession | undefined;
+  getSessionByRoot(root: string): WorkspaceSession | undefined;
   touchSession(id: string): void;
   close?(): void;
 }
@@ -94,6 +95,17 @@ export class SqliteWorkspaceStore implements WorkspaceStore {
     return row ? rowToWorkspaceSession(row) : undefined;
   }
 
+  getSessionByRoot(root: string): WorkspaceSession | undefined {
+    const row = this.database.db
+      .select()
+      .from(workspaceSessions)
+      .where(eq(workspaceSessions.root, root))
+      .orderBy(desc(workspaceSessions.lastUsedAt))
+      .get();
+
+    return row ? rowToWorkspaceSession(row) : undefined;
+  }
+
   touchSession(id: string): void {
     this.database.db
       .update(workspaceSessions)
diff --git a/src/workspaces.test.ts b/src/workspaces.test.ts
index 4f3eb769..f19534c5 100644
--- a/src/workspaces.test.ts
+++ b/src/workspaces.test.ts
@@ -12,6 +12,7 @@ import { ensureCheckoutWorkspaceRoot, WorkspaceRegistry } from "./workspaces.js"
 const execFileAsync = promisify(execFile);
 const root = await mkdtemp(join(tmpdir(), "devspace-workspace-test-"));
 const outsideRoot = await mkdtemp(join(tmpdir(), "devspace-workspace-outside-test-"));
+const worktreeRoot = await mkdtemp(join(tmpdir(), "devspace-worktree-test-"));
 
 try {
   const agentDir = join(root, ".pi", "agent");
@@ -45,7 +46,7 @@ try {
   const config = loadConfig({
     DEVSPACE_CONFIG_DIR: join(root, ".devspace-home"),
     DEVSPACE_ALLOWED_ROOTS: root,
-    DEVSPACE_WORKTREE_ROOT: join(root, ".devspace", "worktrees"),
+    DEVSPACE_WORKTREE_ROOT: worktreeRoot,
     DEVSPACE_AGENT_DIR: agentDir,
     DEVSPACE_SUBAGENTS: "1",
     DEVSPACE_OAUTH_OWNER_TOKEN: "test-owner-token-that-is-long-enough",
@@ -164,6 +165,25 @@ try {
     path: gitRoot,
     mode: "worktree",
   });
+  const persistentWorktreeAgentsDir = join(
+    persistentWorktree.workspace.root,
+    ".devspace",
+    "agents",
+  );
+  await mkdir(persistentWorktreeAgentsDir, { recursive: true });
+  await writeFile(
+    join(persistentWorktreeAgentsDir, "restored.md"),
+    [
+      "---",
+      "name: restored",
+      "description: Available after persisted workspace restoration.",
+      "provider: codex",
+      "---",
+      "",
+      "Restore worktree context.",
+      "",
+    ].join("\n"),
+  );
   firstStore.close();
 
   const secondStore = new SqliteWorkspaceStore(stateDir);
@@ -179,6 +199,27 @@ try {
   assert.equal(restoredWorktree.worktree?.managed, true);
   secondStore.close();
 
+  const reopenedStore = new SqliteWorkspaceStore(stateDir);
+  const reopenedRegistry = new WorkspaceRegistry(config, reopenedStore);
+  try {
+    const reopenedWorktree = await reopenedRegistry.openWorkspace(persistentWorktree.workspace.root);
+    assert.equal(reopenedWorktree.workspace.id, persistentWorktree.workspace.id);
+    assert.equal(reopenedWorktree.workspace.mode, "worktree");
+    assert.equal(reopenedWorktree.workspace.sourceRoot, gitRoot);
+    assert.equal(reopenedWorktree.workspace.root, persistentWorktree.workspace.root);
+    assert.equal(reopenedWorktree.workspace.worktree?.managed, true);
+    assert.deepEqual(
+      reopenedWorktree.workspace.agentProfiles.map((profile) => profile.name),
+      ["restored"],
+    );
+    await assert.rejects(
+      () => reopenedRegistry.openWorkspace(join(worktreeRoot, "unregistered-worktree")),
+      /Path is outside allowed roots/,
+    );
+  } finally {
+    reopenedStore.close();
+  }
+
   if (platform() !== "win32") {
     const aliasRoot = join(root, "alias-root");
     await symlink(root, aliasRoot, "dir");
@@ -204,6 +245,7 @@ try {
 } finally {
   await rm(root, { recursive: true, force: true });
   await rm(outsideRoot, { recursive: true, force: true });
+  await rm(worktreeRoot, { recursive: true, force: true });
 }
 
 async function git(cwd: string, args: string[]): Promise<void> {
diff --git a/src/workspaces.ts b/src/workspaces.ts
index e3c252f4..22744e69 100644
--- a/src/workspaces.ts
+++ b/src/workspaces.ts
@@ -6,7 +6,12 @@ import { dirname, join, relative, resolve, sep } from "node:path";
 import { loadProjectContextFiles } from "@earendil-works/pi-coding-agent";
 import type { ServerConfig } from "./config.js";
 import { createManagedWorktree } from "./git-worktrees.js";
-import { assertAllowedPath, isPathInsideRoot, resolveAllowedPath } from "./roots.js";
+import {
+  assertAllowedPath,
+  expandHomePath,
+  isPathInsideRoot,
+  resolveAllowedPath,
+} from "./roots.js";
 import {
   loadWorkspaceSkills,
   markSkillActivated,
@@ -174,6 +179,15 @@ export class WorkspaceRegistry {
   }
 
   private async openCheckoutWorkspace(path: string): Promise<WorkspaceContext> {
+    const restoredWorktree = this.store?.getSessionByRoot(resolve(expandHomePath(path)));
+    if (restoredWorktree?.mode === "worktree" && restoredWorktree.managed) {
+      const workspace = this.getWorkspace(restoredWorktree.id);
+      workspace.agentProfiles = await loadLocalAgentProfiles(this.config, workspace.root);
+      const agentsFiles = await this.loadInitialAgentsFiles(workspace.root);
+      const availableAgentsFiles = await this.findAvailableAgentsFiles(workspace.root, agentsFiles);
+      return { workspace, agentsFiles, availableAgentsFiles };
+    }
+
     const root = assertAllowedPath(path, this.config.allowedRoots);
     const rootStats = await ensureCheckoutWorkspaceRoot(root);
     if (!rootStats.isDirectory()) {