diff --git a/src/main/index.ts b/src/main/index.ts
index c3069f59..773d7443 100644
--- a/src/main/index.ts
+++ b/src/main/index.ts
@@ -62,6 +62,11 @@ import { ensureOpenCodeBridgeRuntimeBinaryEnv } from '@main/services/runtime/ope
 import { ClaudeMultimodelBridgeService } from '@main/services/runtime/ClaudeMultimodelBridgeService';
 import { applyOpenCodeAutoUpdatePolicy } from '@main/services/runtime/openCodeAutoUpdatePolicy';
 import { providerConnectionService } from '@main/services/runtime/ProviderConnectionService';
+import {
+  computeTeamWatchScope,
+  setAliveTeamsProvider,
+  setTeamWatchScopeChangeListener,
+} from '@main/services/infrastructure/teamWatchScope';
 import { JsonScheduleRepository } from '@main/services/schedule/JsonScheduleRepository';
 import { ScheduledTaskExecutor } from '@main/services/schedule/ScheduledTaskExecutor';
 import { SchedulerService } from '@main/services/schedule/SchedulerService';
@@ -1412,8 +1417,22 @@ function wireFileWatcherEvents(context: ServiceContext): void {
     }
   };
   context.fileWatcher.on('team-change', teamChangeHandler);
+
+  // Scope team-root/task file watching to alive + UI-engaged teams so it no longer
+  // scales with the number of teams on disk. Inboxes and the teams root stay fully
+  // watched, so cross-team delivery, the lead inbox relay, and notifications are
+  // unaffected. Unsetting the provider on cleanup reverts to watching every team.
+  setAliveTeamsProvider(() => teamProvisioningService.getAliveTeamNames());
+  setTeamWatchScopeChangeListener(() => {
+    void context.fileWatcher.refreshTeamWatchScope();
+  });
+  context.fileWatcher.setTeamWatchScopeProvider(() => computeTeamWatchScope());
+  void context.fileWatcher.refreshTeamWatchScope();
+
   teamChangeCleanup = () => {
     context.fileWatcher.off('team-change', teamChangeHandler);
+    setTeamWatchScopeChangeListener(null);
+    context.fileWatcher.setTeamWatchScopeProvider(null);
     reconcileScheduler?.dispose();
   };
 
diff --git a/src/main/ipc/teams.ts b/src/main/ipc/teams.ts
index 64898634..1fe40349 100644
--- a/src/main/ipc/teams.ts
+++ b/src/main/ipc/teams.ts
@@ -4,6 +4,7 @@ import {
 } from '@features/agent-attachments/contracts';
 import { addMainBreadcrumb } from '@main/sentry';
 import { setCurrentMainOp } from '@main/services/infrastructure/EventLoopLagMonitor';
+import { markTeamEngaged } from '@main/services/infrastructure/teamWatchScope';
 import { getTeamDataWorkerClient } from '@main/services/team/TeamDataWorkerClient';
 import { getAppIconPath } from '@main/utils/appIcon';
 import { getAppDataPath, getTeamsBasePath } from '@main/utils/pathDecoder';
@@ -869,6 +870,9 @@ async function handleGetData(
     return { success: false, error: optionsResult.error };
   }
   const tn = validated.value!;
+  // The UI is fetching this team, so keep its team-root/task artifacts watched
+  // (idle teams the UI never opens are not watched, to scale with team count).
+  markTeamEngaged(tn);
   const getDataOptions = optionsResult.value;
   const startedAt = Date.now();
   let data: TeamViewSnapshot;
diff --git a/src/main/services/infrastructure/FileWatcher.ts b/src/main/services/infrastructure/FileWatcher.ts
index 9e2ff08e..05cfe512 100644
--- a/src/main/services/infrastructure/FileWatcher.ts
+++ b/src/main/services/infrastructure/FileWatcher.ts
@@ -94,6 +94,11 @@ export class FileWatcher extends EventEmitter {
   private todosPath: string;
   private teamsPath: string;
   private tasksPath: string;
+  // Optional scope for team-root/task watching (alive ∪ engaged teams). Inboxes
+  // and the teams root are always watched. Null => watch every team (fallback).
+  private teamWatchScopeProvider: (() => ReadonlySet<string> | null) | null = null;
+  private teamsRegistry: TeamTaskWatchRegistry | null = null;
+  private tasksRegistry: TeamTaskWatchRegistry | null = null;
   private dataCache: DataCache;
   private fsProvider: FileSystemProvider;
   private notificationManager: NotificationManager | null = null;
@@ -246,6 +251,31 @@ export class FileWatcher extends EventEmitter {
   /**
    * Sets the filesystem provider. Used when switching between local and SSH modes.
    */
+  /**
+   * Inject the provider that decides which teams' team-root and task artifacts
+   * are watched (typically alive ∪ engaged teams). The teams root and every
+   * team's inboxes are always watched. Returning null (or leaving the provider
+   * unset) watches every team — the safe fallback / original behavior.
+   *
+   * Only the chokidar registry path is scoped; the EMFILE polling fallback still
+   * watches every team so a scope change can never be mistaken for a deletion.
+   */
+  setTeamWatchScopeProvider(provider: (() => ReadonlySet<string> | null) | null): void {
+    this.teamWatchScopeProvider = provider;
+  }
+
+  /**
+   * Recompute the watched team set immediately, e.g. right after a team launches,
+   * stops, or becomes engaged in the UI. Safe to call frequently: it no-ops when
+   * the resolved target set is unchanged and coalesces with in-flight reconciles.
+   */
+  async refreshTeamWatchScope(): Promise<void> {
+    await Promise.all([
+      this.teamsRegistry?.requestReconcile(),
+      this.tasksRegistry?.requestReconcile(),
+    ]);
+  }
+
   setFileSystemProvider(provider: FileSystemProvider): void {
     this.fsProvider = provider;
   }
@@ -545,8 +575,15 @@ export class FileWatcher extends EventEmitter {
         }
       },
       onError,
+      getScopedTeamNames: () => this.teamWatchScopeProvider?.() ?? null,
     });
 
+    if (watcherType === 'teams') {
+      this.teamsRegistry = registry;
+    } else {
+      this.tasksRegistry = registry;
+    }
+
     try {
       await registry.start();
     } catch (error) {
diff --git a/src/main/services/infrastructure/TeamTaskWatchRegistry.ts b/src/main/services/infrastructure/TeamTaskWatchRegistry.ts
index 334279b1..1f259402 100644
--- a/src/main/services/infrastructure/TeamTaskWatchRegistry.ts
+++ b/src/main/services/infrastructure/TeamTaskWatchRegistry.ts
@@ -14,6 +14,20 @@ export interface TeamTaskWatchRegistryOptions {
   rootPath: string;
   onChange: (eventType: TeamTaskWatchEventType, relativePath: string) => void;
   onError: (error: unknown) => void;
+  /**
+   * Optional provider for the set of team names whose team-root and task
+   * artifacts should be watched. The root directory is always watched (to detect
+   * new/removed teams), and for the 'teams' kind every team's `inboxes/` is
+   * always watched (cross-team message delivery and notifications must stay
+   * immediate). Return `null` (or omit the provider) to watch every team — the
+   * original behavior and the safe fallback.
+   *
+   * Scoping exists because team-root (config/kanban/processes/meta) and task
+   * artifacts only change for teams that are running or currently engaged in the
+   * UI; idle teams are static, so watching all of them is pure overhead that
+   * scales with the number of teams on disk.
+   */
+  getScopedTeamNames?: () => ReadonlySet<string> | null;
 }
 
 const RECONCILE_INTERVAL_MS = 30_000;
@@ -76,6 +90,17 @@ export class TeamTaskWatchRegistry {
     this.reconcileTimer.unref();
   }
 
+  /**
+   * Force an immediate target reconciliation. Call this when the scoped team set
+   * changes (a team launches, stops, or becomes engaged in the UI) so the watch
+   * set updates without waiting for the periodic reconcile. Safe to call often:
+   * it no-ops when the resulting target set is unchanged and coalesces with any
+   * in-flight reconcile.
+   */
+  async requestReconcile(): Promise<void> {
+    await this.reconcileTargets();
+  }
+
   async close(): Promise<void> {
     this.closed = true;
     this.generation += 1;
@@ -237,6 +262,8 @@ export class TeamTaskWatchRegistry {
     // emitting user-visible events for those artifacts.
     const targets = new Set<string>([path.normalize(this.options.rootPath)]);
     const rootEntries = await this.readDirectory(this.options.rootPath);
+    // null => no scoping: watch every team (original behavior / safe fallback).
+    const scopedTeams = this.options.getScopedTeamNames?.() ?? null;
 
     for (const entry of rootEntries) {
       if (!entry.isDirectory()) {
@@ -244,7 +271,14 @@ export class TeamTaskWatchRegistry {
       }
 
       const teamPath = path.join(this.options.rootPath, entry.name);
-      targets.add(path.normalize(teamPath));
+      const inScope = scopedTeams === null || scopedTeams.has(entry.name);
+
+      // Team-root and task artifacts only change for running/engaged teams, so
+      // scope those. Inboxes are always watched so cross-team delivery and
+      // notifications to non-visible teams stay immediate.
+      if (inScope) {
+        targets.add(path.normalize(teamPath));
+      }
 
       if (this.options.kind === 'teams') {
         const inboxPath = path.join(teamPath, 'inboxes');
diff --git a/src/main/services/infrastructure/teamWatchScope.ts b/src/main/services/infrastructure/teamWatchScope.ts
new file mode 100644
index 00000000..e553f737
--- /dev/null
+++ b/src/main/services/infrastructure/teamWatchScope.ts
@@ -0,0 +1,82 @@
+/**
+ * Decides which teams' team-root and task artifacts should be file-watched.
+ *
+ * The scope is (teams with a live runtime run) ∪ (teams recently engaged in the
+ * UI). FileWatcher always watches the teams root and every team's `inboxes/`
+ * regardless of this scope, so cross-team message delivery, the lead inbox→stdin
+ * relay, and notifications are unaffected. This module only narrows the heavier
+ * per-team team-root (config/kanban/processes/meta) and task watching, which
+ * otherwise scales with the number of teams on disk and dominates startup cost.
+ *
+ * Module-level state mirrors the existing IPC/registry singletons in this layer.
+ */
+
+const ENGAGED_TTL_MS = 5 * 60_000;
+
+const engagedAtByTeam = new Map<string, number>();
+let aliveTeamsProvider: (() => Iterable<string>) | null = null;
+let scopeChangeListener: (() => void) | null = null;
+
+export function setAliveTeamsProvider(provider: (() => Iterable<string>) | null): void {
+  aliveTeamsProvider = provider;
+}
+
+export function setTeamWatchScopeChangeListener(listener: (() => void) | null): void {
+  scopeChangeListener = listener;
+}
+
+function collectAliveTeams(scope: Set<string>): void {
+  if (!aliveTeamsProvider) {
+    return;
+  }
+  try {
+    for (const teamName of aliveTeamsProvider()) {
+      if (teamName) {
+        scope.add(teamName);
+      }
+    }
+  } catch {
+    // A provider failure must never break watching. The watcher treats a thrown
+    // or empty scope conservatively (inboxes + root stay watched either way).
+  }
+}
+
+/**
+ * Current set of teams whose team-root/task artifacts should be watched. Prunes
+ * engaged entries past their TTL as a side effect of being called.
+ */
+export function computeTeamWatchScope(nowMs: number = Date.now()): ReadonlySet<string> {
+  const scope = new Set<string>();
+  collectAliveTeams(scope);
+  for (const [teamName, engagedAt] of engagedAtByTeam) {
+    if (nowMs - engagedAt <= ENGAGED_TTL_MS) {
+      scope.add(teamName);
+    } else {
+      engagedAtByTeam.delete(teamName);
+    }
+  }
+  return scope;
+}
+
+/**
+ * Mark a team as engaged in the UI (opened or refreshed). Notifies the scope
+ * change listener only when this newly brings the team into scope, so repeated
+ * calls for an already-watched team stay cheap and do not churn the watcher.
+ */
+export function markTeamEngaged(teamName: string, nowMs: number = Date.now()): void {
+  if (!teamName) {
+    return;
+  }
+  const wasInScope = computeTeamWatchScope(nowMs).has(teamName);
+  engagedAtByTeam.set(teamName, nowMs);
+  if (!wasInScope) {
+    scopeChangeListener?.();
+  }
+}
+
+/** Test helper: clear engaged state and wiring. */
+export function resetTeamWatchScopeForTests(): void {
+  engagedAtByTeam.clear();
+  aliveTeamsProvider = null;
+  scopeChangeListener = null;
+}
diff --git a/src/main/services/team/TeamProvisioningService.ts b/src/main/services/team/TeamProvisioningService.ts
index b5cc9314..2cb284ae 100644
--- a/src/main/services/team/TeamProvisioningService.ts
+++ b/src/main/services/team/TeamProvisioningService.ts
@@ -4881,6 +4881,15 @@ export class TeamProvisioningService {
     return this.aliveRunByTeam.get(teamName) ?? null;
   }
 
+  /**
+   * Snapshot of teams that currently have a live runtime run. Used to keep the
+   * file-watch scope covering running teams (read-only; the map is maintained as
+   * runs start and stop).
+   */
+  getAliveTeamNames(): string[] {
+    return [...this.aliveRunByTeam.keys()];
+  }
+
   private getTrackedRunId(teamName: string): string | null {
     return this.getProvisioningRunId(teamName) ?? this.getAliveRunId(teamName);
   }
diff --git a/test/main/services/infrastructure/TeamTaskWatchRegistry.test.ts b/test/main/services/infrastructure/TeamTaskWatchRegistry.test.ts
new file mode 100644
index 00000000..2076fc5c
--- /dev/null
+++ b/test/main/services/infrastructure/TeamTaskWatchRegistry.test.ts
@@ -0,0 +1,159 @@
+import * as fs from 'fs';
+import * as os from 'os';
+import * as path from 'path';
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest';
+
+type MockChokidarWatcher = {
+  targets: string[];
+  options: unknown;
+  on: (event: string, handler: (...args: unknown[]) => void) => MockChokidarWatcher;
+  close: ReturnType<typeof vi.fn>;
+};
+
+const chokidarMock = vi.hoisted(() => {
+  const instances: MockChokidarWatcher[] = [];
+  const make = () => (targets: string | string[], options: unknown) => {
+    const watcher = {
+      targets: (Array.isArray(targets) ? targets : [targets]).map((t) => String(t)),
+      options,
+      close: vi.fn().mockResolvedValue(undefined),
+    } as MockChokidarWatcher;
+    watcher.on = vi.fn(() => watcher);
+    instances.push(watcher);
+    return watcher;
+  };
+  const watch = vi.fn(make());
+  return {
+    instances,
+    watch,
+    reset() {
+      instances.length = 0;
+      watch.mockReset();
+      watch.mockImplementation(make());
+    },
+  };
+});
+
+vi.mock('chokidar', () => ({ watch: chokidarMock.watch }));
+
+import { TeamTaskWatchRegistry } from '../../../../src/main/services/infrastructure/TeamTaskWatchRegistry';
+
+function latestTargets(): string[] {
+  const last = chokidarMock.instances.at(-1);
+  return (last?.targets ?? []).map((t) => path.normalize(t));
+}
+
+describe('TeamTaskWatchRegistry scoping', () => {
+  let root: string;
+
+  beforeEach(() => {
+    chokidarMock.reset();
+    root = fs.mkdtempSync(path.join(os.tmpdir(), 'ttwr-scope-'));
+    for (const team of ['alpha', 'beta', 'gamma']) {
+      fs.mkdirSync(path.join(root, team, 'inboxes'), { recursive: true });
+      fs.writeFileSync(path.join(root, team, 'config.json'), '{}');
+      fs.writeFileSync(path.join(root, team, 'inboxes', 'team-lead.json'), '[]');
+    }
+  });
+
+  afterEach(() => {
+    fs.rmSync(root, { recursive: true, force: true });
+  });
+
+  it('watches only scoped team dirs but every team inbox (teams kind)', async () => {
+    const registry = new TeamTaskWatchRegistry({
+      kind: 'teams',
+      rootPath: root,
+      onChange: () => {},
+      onError: () => {},
+      getScopedTeamNames: () => new Set(['alpha']),
+    });
+    await registry.start();
+    const targets = latestTargets();
+    await registry.close();
+
+    expect(targets).toContain(path.normalize(root));
+    // scoped team root watched, unscoped team roots not watched
+    expect(targets).toContain(path.normalize(path.join(root, 'alpha')));
+    expect(targets).not.toContain(path.normalize(path.join(root, 'beta')));
+    expect(targets).not.toContain(path.normalize(path.join(root, 'gamma')));
+    // ALL inboxes watched regardless of scope (cross-team delivery)
+    expect(targets).toContain(path.normalize(path.join(root, 'alpha', 'inboxes')));
+    expect(targets).toContain(path.normalize(path.join(root, 'beta', 'inboxes')));
+    expect(targets).toContain(path.normalize(path.join(root, 'gamma', 'inboxes')));
+  });
+
+  it('falls back to watching every team when no scope provider is given', async () => {
+    const registry = new TeamTaskWatchRegistry({
+      kind: 'teams',
+      rootPath: root,
+      onChange: () => {},
+      onError: () => {},
+    });
+    await registry.start();
+    const targets = latestTargets();
+    await registry.close();
+
+    for (const team of ['alpha', 'beta', 'gamma']) {
+      expect(targets).toContain(path.normalize(path.join(root, team)));
+      expect(targets).toContain(path.normalize(path.join(root, team, 'inboxes')));
+    }
+  });
+
+  it('falls back to watching every team when the scope provider returns null', async () => {
+    const registry = new TeamTaskWatchRegistry({
+      kind: 'teams',
+      rootPath: root,
+      onChange: () => {},
+      onError: () => {},
+      getScopedTeamNames: () => null,
+    });
+    await registry.start();
+    const targets = latestTargets();
+    await registry.close();
+
+    for (const team of ['alpha', 'beta', 'gamma']) {
+      expect(targets).toContain(path.normalize(path.join(root, team)));
+    }
+  });
+
+  it('scopes task dirs and never adds inboxes (tasks kind)', async () => {
+    const registry = new TeamTaskWatchRegistry({
+      kind: 'tasks',
+      rootPath: root,
+      onChange: () => {},
+      onError: () => {},
+      getScopedTeamNames: () => new Set(['beta']),
+    });
+    await registry.start();
+    const targets = latestTargets();
+    await registry.close();
+
+    expect(targets).toContain(path.normalize(root));
+    expect(targets).toContain(path.normalize(path.join(root, 'beta')));
+    expect(targets).not.toContain(path.normalize(path.join(root, 'alpha')));
+    expect(targets).not.toContain(path.normalize(path.join(root, 'gamma')));
+    // tasks kind never watches inboxes
+    expect(targets).not.toContain(path.normalize(path.join(root, 'beta', 'inboxes')));
+  });
+
+  it('re-resolves scope on requestReconcile (newly scoped team gets watched)', async () => {
+    const scoped = new Set<string>(['alpha']);
+    const registry = new TeamTaskWatchRegistry({
+      kind: 'teams',
+      rootPath: root,
+      onChange: () => {},
+      onError: () => {},
+      getScopedTeamNames: () => scoped,
+    });
+    await registry.start();
+    expect(latestTargets()).not.toContain(path.normalize(path.join(root, 'beta')));
+
+    scoped.add('beta');
+    await registry.requestReconcile();
+    const targets = latestTargets();
+    await registry.close();
+
+    expect(targets).toContain(path.normalize(path.join(root, 'beta')));
+  });
+});
diff --git a/test/main/services/infrastructure/teamWatchScope.test.ts b/test/main/services/infrastructure/teamWatchScope.test.ts
new file mode 100644
index 00000000..70446671
--- /dev/null
+++ b/test/main/services/infrastructure/teamWatchScope.test.ts
@@ -0,0 +1,71 @@
+import { afterEach, describe, expect, it, vi } from 'vitest';
+
+import {
+  computeTeamWatchScope,
+  markTeamEngaged,
+  resetTeamWatchScopeForTests,
+  setAliveTeamsProvider,
+  setTeamWatchScopeChangeListener,
+} from '../../../../src/main/services/infrastructure/teamWatchScope';
+
+const FIVE_MIN = 5 * 60_000;
+
+afterEach(() => {
+  resetTeamWatchScopeForTests();
+});
+
+describe('teamWatchScope', () => {
+  it('includes alive teams from the provider', () => {
+    setAliveTeamsProvider(() => ['t-alive']);
+    expect([...computeTeamWatchScope(1000)]).toContain('t-alive');
+  });
+
+  it('includes engaged teams within TTL and prunes after expiry', () => {
+    markTeamEngaged('t-eng', 0);
+    expect(computeTeamWatchScope(FIVE_MIN).has('t-eng')).toBe(true);
+    expect(computeTeamWatchScope(FIVE_MIN + 1).has('t-eng')).toBe(false);
+    // pruning is sticky: it stays out without re-engaging
+    expect(computeTeamWatchScope(FIVE_MIN + 2).has('t-eng')).toBe(false);
+  });
+
+  it('unions alive and engaged teams', () => {
+    setAliveTeamsProvider(() => ['a']);
+    markTeamEngaged('b', 0);
+    const scope = computeTeamWatchScope(1000);
+    expect(scope.has('a')).toBe(true);
+    expect(scope.has('b')).toBe(true);
+  });
+
+  it('notifies the listener only when engagement newly adds to scope', () => {
+    const listener = vi.fn();
+    setTeamWatchScopeChangeListener(listener);
+    markTeamEngaged('x', 0);
+    expect(listener).toHaveBeenCalledTimes(1);
+    markTeamEngaged('x', 1000); // already in scope -> no extra churn
+    expect(listener).toHaveBeenCalledTimes(1);
+  });
+
+  it('does not notify when engaging an already-alive (in-scope) team', () => {
+    setAliveTeamsProvider(() => ['y']);
+    const listener = vi.fn();
+    setTeamWatchScopeChangeListener(listener);
+    markTeamEngaged('y', 0);
+    expect(listener).not.toHaveBeenCalled();
+  });
+
+  it('survives a throwing alive provider (watcher falls back safely)', () => {
+    setAliveTeamsProvider(() => {
+      throw new Error('boom');
+    });
+    expect(() => computeTeamWatchScope(0)).not.toThrow();
+    expect([...computeTeamWatchScope(0)]).toEqual([]);
+  });
+
+  it('ignores empty team names', () => {
+    const listener = vi.fn();
+    setTeamWatchScopeChangeListener(listener);
+    markTeamEngaged('', 0);
+    expect(listener).not.toHaveBeenCalled();
+    expect(computeTeamWatchScope(0).size).toBe(0);
+  });
+});