diff --git a/test/test.workapp-mail-manager.node.ts b/test/test.workapp-mail-manager.node.ts
new file mode 100644
index 0000000..c78e88f
--- /dev/null
+++ b/test/test.workapp-mail-manager.node.ts
@@ -0,0 +1,175 @@
+import { tap, expect } from '@git.zone/tstest/tapbundle';
+import { WorkAppMailManager } from '../ts/email/classes.workapp-mail-manager.js';
+import type { IUnifiedEmailServerOptions } from '@push.rocks/smartmta';
+
+class MemoryStorageManager {
+  public store = new Map<string, string>();
+
+  public async get(key: string): Promise<string | null> {
+    return this.store.get(key) || null;
+  }
+
+  public async set(key: string, value: string): Promise<void> {
+    this.store.set(key, value);
+  }
+}
+
+const createDcRouterStub = () => {
+  const storageManager = new MemoryStorageManager();
+  const emailConfig: IUnifiedEmailServerOptions = {
+    hostname: 'mail.example.com',
+    ports: [25, 587, 465],
+    domains: [
+      {
+        domain: 'example.com',
+        dnsMode: 'external-dns',
+      },
+    ],
+    routes: [
+      {
+        name: 'operator-route',
+        match: { recipients: 'ops@example.com' },
+        action: { type: 'reject', reject: { code: 550, message: 'not here' } },
+      },
+    ],
+    auth: {
+      users: [{ username: 'operator', password: 'secret' }],
+    },
+  };
+  const dcRouterRef: any = {
+    storageManager,
+    options: { emailConfig },
+    emailServer: {
+      updateOptions: (patch: Partial<IUnifiedEmailServerOptions>) => {
+        dcRouterRef.options.emailConfig = {
+          ...dcRouterRef.options.emailConfig,
+          ...patch,
+        };
+      },
+    },
+    updateEmailRoutes: async (routes: IUnifiedEmailServerOptions['routes']) => {
+      dcRouterRef.options.emailConfig.routes = routes;
+    },
+  };
+  return { dcRouterRef, storageManager };
+};
+
+tap.test('WorkAppMailManager syncs SMTP identity and inbound smartmta route', async () => {
+  const { dcRouterRef } = createDcRouterStub();
+  const manager = new WorkAppMailManager(dcRouterRef);
+
+  const createResult = await manager.syncMailIdentity({
+    ownership: {
+      workHosterType: 'onebox',
+      workHosterId: 'box-1',
+      workAppId: 'app-1',
+    },
+    localPart: 'Hello',
+    domain: 'Example.com',
+    inbound: {
+      enabled: true,
+      targetHost: '10.0.0.2',
+      targetPort: 2525,
+    },
+  }, 'tester');
+
+  expect(createResult.success).toEqual(true);
+  expect(createResult.action).toEqual('created');
+  expect(createResult.identity?.address).toEqual('hello@example.com');
+  expect(createResult.identity?.smtp.username.startsWith('workapp-')).toEqual(true);
+  expect((createResult.identity as any).smtpPassword).toBeUndefined();
+  expect(createResult.smtpCredentials?.password.length).toBeGreaterThan(20);
+
+  const generatedRoute = dcRouterRef.options.emailConfig.routes.find((route: any) => route.name.startsWith('workapp-mail-'));
+  expect(generatedRoute.match.recipients).toEqual('hello@example.com');
+  expect(generatedRoute.action.forward.host).toEqual('10.0.0.2');
+  expect(generatedRoute.action.forward.port).toEqual(2525);
+  expect(generatedRoute.action.forward.addHeaders['X-Dcrouter-WorkApp-Id']).toEqual('app-1');
+  expect(dcRouterRef.options.emailConfig.routes.some((route: any) => route.name === 'operator-route')).toEqual(true);
+
+  const generatedUser = dcRouterRef.options.emailConfig.auth.users.find((user: any) => user.username.startsWith('workapp-'));
+  expect(generatedUser.password).toEqual(createResult.smtpCredentials?.password);
+  expect(dcRouterRef.options.emailConfig.auth.users.some((user: any) => user.username === 'operator')).toEqual(true);
+
+  const listResult = await manager.listMailIdentities({ workAppId: 'app-1' });
+  expect(listResult.length).toEqual(1);
+  expect(listResult[0].address).toEqual('hello@example.com');
+});
+
+tap.test('WorkAppMailManager updates, resets credentials, and deletes identities', async () => {
+  const { dcRouterRef } = createDcRouterStub();
+  const manager = new WorkAppMailManager(dcRouterRef);
+  const ownership = {
+    workHosterType: 'onebox' as const,
+    workHosterId: 'box-1',
+    workAppId: 'app-1',
+  };
+
+  const createResult = await manager.syncMailIdentity({
+    ownership,
+    localPart: 'hello',
+    domain: 'example.com',
+    inbound: { enabled: true, targetHost: '10.0.0.2', targetPort: 2525 },
+  }, 'tester');
+  const firstPassword = createResult.smtpCredentials!.password;
+
+  const updateResult = await manager.syncMailIdentity({
+    ownership,
+    localPart: 'hello',
+    domain: 'example.com',
+    inbound: { enabled: true, targetHost: '10.0.0.3', targetPort: 2526 },
+  }, 'tester');
+  expect(updateResult.action).toEqual('updated');
+  expect(updateResult.smtpCredentials).toBeUndefined();
+  const generatedUser = dcRouterRef.options.emailConfig.auth.users.find((user: any) => user.username.startsWith('workapp-'));
+  expect(generatedUser.password).toEqual(firstPassword);
+  const generatedRoute = dcRouterRef.options.emailConfig.routes.find((route: any) => route.name.startsWith('workapp-mail-'));
+  expect(generatedRoute.action.forward.host).toEqual('10.0.0.3');
+
+  const resetResult = await manager.syncMailIdentity({
+    ownership,
+    localPart: 'hello',
+    domain: 'example.com',
+    resetSmtpPassword: true,
+  }, 'tester');
+  expect(resetResult.smtpCredentials?.password !== firstPassword).toEqual(true);
+
+  const deleteResult = await manager.syncMailIdentity({
+    ownership,
+    localPart: 'hello',
+    domain: 'example.com',
+    delete: true,
+  }, 'tester');
+  expect(deleteResult.action).toEqual('deleted');
+  expect(dcRouterRef.options.emailConfig.routes.some((route: any) => route.name.startsWith('workapp-mail-'))).toEqual(false);
+  expect(dcRouterRef.options.emailConfig.auth.users.some((user: any) => user.username.startsWith('workapp-'))).toEqual(false);
+  expect(dcRouterRef.options.emailConfig.auth.users.some((user: any) => user.username === 'operator')).toEqual(true);
+});
+
+tap.test('WorkAppMailManager applies persisted identities to startup email config', async () => {
+  const { dcRouterRef } = createDcRouterStub();
+  const manager = new WorkAppMailManager(dcRouterRef);
+  await manager.syncMailIdentity({
+    ownership: {
+      workHosterType: 'onebox',
+      workHosterId: 'box-1',
+      workAppId: 'app-1',
+    },
+    localPart: 'hello',
+    domain: 'example.com',
+    inbound: { enabled: true, targetHost: '10.0.0.2', targetPort: 2525 },
+  }, 'tester');
+
+  const baseStartupConfig: IUnifiedEmailServerOptions = {
+    hostname: 'mail.example.com',
+    ports: [25],
+    domains: [{ domain: 'example.com', dnsMode: 'external-dns' }],
+    routes: [],
+  };
+  const startupConfig = await manager.applyStoredIdentitiesToEmailConfig(baseStartupConfig);
+
+  expect(startupConfig.routes.some((route) => route.name.startsWith('workapp-mail-'))).toEqual(true);
+  expect(startupConfig.auth?.users?.some((user) => user.username.startsWith('workapp-'))).toEqual(true);
+});
+
+export default tap.start();
diff --git a/test/test.workhoster-handler.node.ts b/test/test.workhoster-handler.node.ts
index 35d64b0..8b51153 100644
--- a/test/test.workhoster-handler.node.ts
+++ b/test/test.workhoster-handler.node.ts
@@ -285,4 +285,98 @@ tap.test('WorkHosterHandler rejects WorkApp route sync without workhosters:write
   expect(routeConfig.routes.size).toEqual(0);
 });
 
+tap.test('WorkHosterHandler exposes and syncs WorkApp mail identities', async () => {
+  const syncedRequests: Array<{ data: any; userId: string }> = [];
+  const identity: interfaces.data.IWorkAppMailIdentity = {
+    id: 'mail-1',
+    externalKey: 'onebox:box-1:app-1:hello@example.com',
+    ownership: {
+      workHosterType: 'onebox',
+      workHosterId: 'box-1',
+      workAppId: 'app-1',
+    },
+    address: 'hello@example.com',
+    localPart: 'hello',
+    domain: 'example.com',
+    enabled: true,
+    inbound: {
+      enabled: true,
+      targetHost: '10.0.0.2',
+      targetPort: 2525,
+    },
+    smtp: {
+      enabled: true,
+      username: 'workapp-user',
+    },
+    createdAt: 1,
+    updatedAt: 1,
+    createdBy: 'token-user',
+  };
+  const { typedrouter } = setupHandler({
+    scopes: ['workhosters:read', 'workhosters:write'],
+    dcRouterRef: {
+      options: {},
+      workAppMailManager: {
+        listMailIdentities: async (filter: any) => filter.workAppId === 'app-1' ? [identity] : [],
+        syncMailIdentity: async (data: any, userId: string) => {
+          syncedRequests.push({ data, userId });
+          return {
+            success: true,
+            action: 'created',
+            identity,
+            smtpCredentials: {
+              username: 'workapp-user',
+              password: 'generated-password',
+            },
+          };
+        },
+      },
+    },
+  });
+
+  const listResult = await fireTypedRequest(typedrouter, 'getWorkAppMailIdentities', {
+    apiToken: 'valid-token',
+    ownership: { workAppId: 'app-1' },
+  });
+  expect(listResult.error).toBeUndefined();
+  expect(listResult.response.identities).toEqual([identity]);
+
+  const syncResult = await fireTypedRequest(typedrouter, 'syncWorkAppMailIdentity', {
+    apiToken: 'valid-token',
+    ownership: identity.ownership,
+    localPart: 'hello',
+    domain: 'example.com',
+    inbound: identity.inbound,
+  });
+  expect(syncResult.error).toBeUndefined();
+  expect(syncResult.response.success).toEqual(true);
+  expect(syncResult.response.smtpCredentials.password).toEqual('generated-password');
+  expect(syncedRequests[0].userId).toEqual('token-user');
+});
+
+tap.test('WorkHosterHandler rejects WorkApp mail sync without workhosters:write', async () => {
+  const { typedrouter } = setupHandler({
+    scopes: ['workhosters:read'],
+    dcRouterRef: {
+      options: {},
+      workAppMailManager: {
+        syncMailIdentity: async () => ({ success: true }),
+      },
+    },
+  });
+
+  const result = await fireTypedRequest(typedrouter, 'syncWorkAppMailIdentity', {
+    apiToken: 'valid-token',
+    ownership: {
+      workHosterType: 'onebox',
+      workHosterId: 'box-1',
+      workAppId: 'app-1',
+    },
+    localPart: 'hello',
+    domain: 'example.com',
+  });
+
+  expect(result.error?.text).toEqual('insufficient scope');
+});
+
 export default tap.start();
diff --git a/ts/classes.dcrouter.ts b/ts/classes.dcrouter.ts
index 91b5b0d..3dd5875 100644
--- a/ts/classes.dcrouter.ts
+++ b/ts/classes.dcrouter.ts
@@ -31,7 +31,7 @@ import { SecurityLogger, ContentScanner, IPReputationChecker, SecurityPolicyMana
 import { type IHttp3Config, augmentRoutesWithHttp3 } from './http3/index.js';
 import { DnsManager } from './dns/manager.dns.js';
 import { AcmeConfigManager } from './acme/manager.acme-config.js';
-import { EmailDomainManager, SmartMtaStorageManager, buildEmailDnsRecords } from './email/index.js';
+import { EmailDomainManager, SmartMtaStorageManager, WorkAppMailManager, buildEmailDnsRecords } from './email/index.js';
 import type { IRoute } from '../ts_interfaces/data/route-management.js';
 import type { ISecurityCompiledPolicy } from '../ts_interfaces/data/security-policy.js';
 
@@ -285,6 +285,7 @@ export class DcRouter {
   // ACME configuration (DB-backed singleton, replaces tls.contactEmail)
   public acmeConfigManager?: AcmeConfigManager;
   public emailDomainManager?: EmailDomainManager;
+  public workAppMailManager: WorkAppMailManager;
   public securityPolicyManager?: SecurityPolicyManager;
 
   // Auto-discovered public IP (populated by generateAuthoritativeRecords)
@@ -339,6 +340,7 @@ export class DcRouter {
     this.storageManager = new SmartMtaStorageManager(
       plugins.path.join(this.resolvedPaths.dataDir, 'smartmta-storage')
     );
+    this.workAppMailManager = new WorkAppMailManager(this);
 
     // Initialize service manager and register all services
     this.serviceManager = new plugins.taskbuffer.ServiceManager({
@@ -1630,7 +1632,7 @@ export class DcRouter {
     }
     
     // Create config with mapped ports
-    const emailConfig: IUnifiedEmailServerOptions = {
+    const emailConfig: IUnifiedEmailServerOptions = await this.workAppMailManager.applyStoredIdentitiesToEmailConfig({
       ...this.options.emailConfig,
       domains: transformedDomains,
       ports: this.options.emailConfig.ports.map(port => portMapping[port] || port + 10000),
@@ -1640,7 +1642,7 @@ export class DcRouter {
         persistentPath: plugins.path.join(this.resolvedPaths.dataDir, 'smartmta-queue'),
         ...this.options.emailConfig.queue,
       },
-    };
+    });
     
     // Create unified email server
     this.emailServer = new UnifiedEmailServer(this, emailConfig);
diff --git a/ts/email/classes.email-domain.manager.ts b/ts/email/classes.email-domain.manager.ts
index 9d02fab..8c8325b 100644
--- a/ts/email/classes.email-domain.manager.ts
+++ b/ts/email/classes.email-domain.manager.ts
@@ -57,6 +57,31 @@ export class EmailDomainManager {
     return doc ? this.docToInterface(doc) : null;
   }
 
+  public async getByDomain(domainName: string): Promise<IEmailDomain | null> {
+    const doc = await EmailDomainDoc.findByDomain(domainName);
+    return doc ? this.docToInterface(doc) : null;
+  }
+
+  public async ensureEmailDomainForDomainName(domainName: string): Promise<IEmailDomain | null> {
+    const normalizedDomain = domainName.trim().toLowerCase();
+    const existing = await this.getByDomain(normalizedDomain);
+    if (existing) return existing;
+    if (this.isDomainAlreadyConfigured(normalizedDomain)) return null;
+
+    const linkedDomain = await this.findLinkedDnsDomain(normalizedDomain);
+    if (!linkedDomain) {
+      throw new Error(`DNS domain not found for email domain: ${normalizedDomain}`);
+    }
+
+    const subdomain = normalizedDomain === linkedDomain.name
+      ? undefined
+      : normalizedDomain.slice(0, -(linkedDomain.name.length + 1));
+    return await this.createEmailDomain({
+      linkedDomainId: linkedDomain.id,
+      subdomain,
+    });
+  }
+
   public async createEmailDomain(opts: {
     linkedDomainId: string;
     subdomain?: string;
@@ -351,6 +376,13 @@ export class EmailDomainManager {
     return configuredDomains.includes(domainName.toLowerCase());
   }
 
+  private async findLinkedDnsDomain(domainName: string): Promise<DomainDoc | null> {
+    const domains = await DomainDoc.findAll();
+    return domains
+      .filter((domainDoc) => domainName === domainDoc.name || domainName.endsWith(`.${domainDoc.name}`))
+      .sort((a, b) => b.name.length - a.name.length)[0] || null;
+  }
+
   private async buildManagedDomainConfigs(): Promise<IEmailDomainConfig[]> {
     const docs = await EmailDomainDoc.findAll();
     const managedConfigs: IEmailDomainConfig[] = [];
@@ -378,7 +410,7 @@ export class EmailDomainManager {
     return managedConfigs;
   }
 
-  private async syncManagedDomainsToRuntime(): Promise<void> {
+  public async syncManagedDomainsToRuntime(): Promise<void> {
     if (!this.dcRouter.options?.emailConfig) {
       return;
     }
diff --git a/ts/email/classes.workapp-mail-manager.ts b/ts/email/classes.workapp-mail-manager.ts
new file mode 100644
index 0000000..87b57eb
--- /dev/null
+++ b/ts/email/classes.workapp-mail-manager.ts
@@ -0,0 +1,343 @@
+import type {
+  IEmailRoute,
+  IUnifiedEmailServerOptions,
+} from '@push.rocks/smartmta';
+import * as plugins from '../plugins.js';
+import type * as interfaces from '../../ts_interfaces/index.js';
+
+type TSyncRequest = interfaces.requests.IReq_SyncWorkAppMailIdentity['request'];
+
+interface IStoredWorkAppMailIdentity extends interfaces.data.IWorkAppMailIdentity {
+  smtpPassword: string;
+}
+
+interface IStoredWorkAppMailState {
+  version: 1;
+  identities: IStoredWorkAppMailIdentity[];
+}
+
+export class WorkAppMailManager {
+  private readonly storageKey = '/workhosters/mail-identities.json';
+
+  constructor(private dcRouterRef: any) {}
+
+  public async listMailIdentities(
+    ownership?: Partial<interfaces.data.IWorkAppMailOwnership>,
+  ): Promise<interfaces.data.IWorkAppMailIdentity[]> {
+    const identities = await this.readStoredIdentities();
+    return identities
+      .filter((identity) => this.matchesOwnership(identity.ownership, ownership))
+      .map((identity) => this.toPublicIdentity(identity));
+  }
+
+  public async syncMailIdentity(
+    request: TSyncRequest,
+    createdBy: string,
+  ): Promise<interfaces.data.IWorkAppMailIdentitySyncResult> {
+    if (!this.dcRouterRef.options.emailConfig) {
+      return { success: false, message: 'Email server is not configured' };
+    }
+
+    const ownership = this.normalizeOwnership(request.ownership);
+    const domain = this.normalizeDomain(request.domain);
+    const localPart = this.normalizeLocalPart(request.localPart);
+    const address = `${localPart}@${domain}`;
+    const externalKey = this.buildExternalKey(ownership, address);
+    const identities = await this.readStoredIdentities();
+    const existingIndex = identities.findIndex((identity) => identity.externalKey === externalKey);
+
+    if (request.delete) {
+      if (existingIndex < 0) {
+        return { success: true, action: 'unchanged' };
+      }
+      const [deletedIdentity] = identities.splice(existingIndex, 1);
+      await this.writeStoredIdentities(identities);
+      await this.applyStoredIdentitiesToRuntime(identities);
+      return {
+        success: true,
+        action: 'deleted',
+        identity: this.toPublicIdentity(deletedIdentity),
+      };
+    }
+
+    await this.ensureEmailDomainConfigured(domain);
+
+    const existingIdentity = existingIndex >= 0 ? identities[existingIndex] : undefined;
+    const now = Date.now();
+    const smtpPassword = existingIdentity && !request.resetSmtpPassword
+      ? existingIdentity.smtpPassword
+      : this.generateSmtpPassword();
+    const identity: IStoredWorkAppMailIdentity = {
+      id: existingIdentity?.id || plugins.smartunique.shortId(),
+      externalKey,
+      ownership,
+      address,
+      localPart,
+      domain,
+      enabled: request.enabled ?? existingIdentity?.enabled ?? true,
+      displayName: request.displayName ?? existingIdentity?.displayName,
+      inbound: this.normalizeInboundRoute(request.inbound ?? existingIdentity?.inbound),
+      smtp: {
+        enabled: request.smtpEnabled ?? existingIdentity?.smtp.enabled ?? true,
+        username: existingIdentity?.smtp.username || this.buildSmtpUsername(externalKey),
+      },
+      createdAt: existingIdentity?.createdAt || now,
+      updatedAt: now,
+      createdBy: existingIdentity?.createdBy || createdBy,
+      smtpPassword,
+    };
+
+    if (existingIndex >= 0) {
+      identities[existingIndex] = identity;
+    } else {
+      identities.push(identity);
+    }
+
+    await this.writeStoredIdentities(identities);
+    await this.applyStoredIdentitiesToRuntime(identities);
+
+    const response: interfaces.data.IWorkAppMailIdentitySyncResult = {
+      success: true,
+      action: existingIndex >= 0 ? 'updated' : 'created',
+      identity: this.toPublicIdentity(identity),
+    };
+
+    if (existingIndex < 0 || request.resetSmtpPassword) {
+      response.smtpCredentials = this.buildSmtpCredentials(identity);
+    }
+
+    return response;
+  }
+
+  public async applyStoredIdentitiesToEmailConfig<TConfig extends IUnifiedEmailServerOptions>(
+    emailConfig: TConfig,
+  ): Promise<TConfig> {
+    const identities = await this.readStoredIdentities();
+    return this.mergeIdentitiesIntoEmailConfig(emailConfig, identities);
+  }
+
+  public async applyStoredIdentitiesToRuntime(
+    identities = undefined as IStoredWorkAppMailIdentity[] | undefined,
+  ): Promise<void> {
+    const emailConfig = this.dcRouterRef.options.emailConfig as IUnifiedEmailServerOptions | undefined;
+    if (!emailConfig) return;
+
+    const nextConfig = this.mergeIdentitiesIntoEmailConfig(
+      emailConfig,
+      identities || await this.readStoredIdentities(),
+    );
+
+    this.dcRouterRef.options.emailConfig = nextConfig;
+    if (this.dcRouterRef.emailServer) {
+      this.dcRouterRef.emailServer.updateOptions({ auth: nextConfig.auth });
+      await this.dcRouterRef.updateEmailRoutes(nextConfig.routes);
+    }
+  }
+
+  private async readStoredIdentities(): Promise<IStoredWorkAppMailIdentity[]> {
+    const storedData = await this.dcRouterRef.storageManager.get(this.storageKey);
+    if (!storedData) return [];
+    const parsed = JSON.parse(storedData) as IStoredWorkAppMailState | IStoredWorkAppMailIdentity[];
+    return Array.isArray(parsed) ? parsed : parsed.identities || [];
+  }
+
+  private async writeStoredIdentities(identities: IStoredWorkAppMailIdentity[]): Promise<void> {
+    const state: IStoredWorkAppMailState = {
+      version: 1,
+      identities,
+    };
+    await this.dcRouterRef.storageManager.set(this.storageKey, JSON.stringify(state, null, 2));
+  }
+
+  private mergeIdentitiesIntoEmailConfig<TConfig extends IUnifiedEmailServerOptions>(
+    emailConfig: TConfig,
+    identities: IStoredWorkAppMailIdentity[],
+  ): TConfig {
+    const generatedRoutes = identities
+      .filter((identity) => identity.enabled && identity.inbound?.enabled)
+      .map((identity) => this.buildInboundRoute(identity));
+    const configuredRoutes = (emailConfig.routes || [])
+      .filter((route) => !this.isManagedMailRouteName(route.name));
+    const generatedUsers = identities
+      .filter((identity) => identity.enabled && identity.smtp.enabled)
+      .map((identity) => ({
+        username: identity.smtp.username,
+        password: identity.smtpPassword,
+      }));
+    const configuredUsers = (emailConfig.auth?.users || [])
+      .filter((user) => !this.isManagedSmtpUsername(user.username));
+
+    return {
+      ...emailConfig,
+      routes: [...configuredRoutes, ...generatedRoutes],
+      auth: {
+        ...(emailConfig.auth || {}),
+        users: [...configuredUsers, ...generatedUsers],
+      },
+    };
+  }
+
+  private buildInboundRoute(identity: IStoredWorkAppMailIdentity): IEmailRoute {
+    const inbound = identity.inbound!;
+    return {
+      name: this.buildRouteName(identity.externalKey),
+      priority: 1000,
+      match: {
+        recipients: identity.address,
+      },
+      action: {
+        type: 'forward',
+        forward: {
+          host: inbound.targetHost,
+          port: inbound.targetPort,
+          preserveHeaders: inbound.preserveHeaders ?? true,
+          addHeaders: {
+            'X-Dcrouter-WorkHoster-Type': identity.ownership.workHosterType,
+            'X-Dcrouter-WorkHoster-Id': identity.ownership.workHosterId,
+            'X-Dcrouter-WorkApp-Id': identity.ownership.workAppId,
+            ...(inbound.addHeaders || {}),
+          },
+        },
+      },
+    };
+  }
+
+  private async ensureEmailDomainConfigured(domain: string): Promise<void> {
+    const emailConfig = this.dcRouterRef.options.emailConfig as IUnifiedEmailServerOptions | undefined;
+    if (emailConfig?.domains?.some((domainConfig) => domainConfig.domain.toLowerCase() === domain)) {
+      return;
+    }
+
+    const emailDomainManager = this.dcRouterRef.emailDomainManager;
+    if (!emailDomainManager) {
+      throw new Error(`Email domain is not configured: ${domain}`);
+    }
+
+    if (await emailDomainManager.getByDomain(domain)) {
+      await emailDomainManager.syncManagedDomainsToRuntime();
+      return;
+    }
+
+    await emailDomainManager.ensureEmailDomainForDomainName(domain);
+  }
+
+  private normalizeOwnership(
+    ownership: interfaces.data.IWorkAppMailOwnership,
+  ): interfaces.data.IWorkAppMailOwnership {
+    const workHosterType = ownership.workHosterType;
+    const workHosterId = ownership.workHosterId?.trim();
+    const workAppId = ownership.workAppId?.trim();
+    if (!['onebox', 'cloudly', 'custom'].includes(workHosterType)) {
+      throw new Error(`Invalid WorkHoster type: ${workHosterType}`);
+    }
+    if (!workHosterId) throw new Error('workHosterId is required');
+    if (!workAppId) throw new Error('workAppId is required');
+    return { workHosterType, workHosterId, workAppId };
+  }
+
+  private normalizeDomain(domain: string): string {
+    const normalized = domain?.trim().toLowerCase();
+    if (!normalized || normalized.includes('@') || !normalized.includes('.')) {
+      throw new Error(`Invalid email domain: ${domain}`);
+    }
+    return normalized;
+  }
+
+  private normalizeLocalPart(localPart: string): string {
+    const normalized = localPart?.trim().toLowerCase();
+    if (!normalized || normalized.includes('@') || /\s/.test(normalized)) {
+      throw new Error(`Invalid email local part: ${localPart}`);
+    }
+    return normalized;
+  }
+
+  private normalizeInboundRoute(
+    inbound?: interfaces.data.IWorkAppMailInboundRoute,
+  ): interfaces.data.IWorkAppMailInboundRoute | undefined {
+    if (!inbound) return undefined;
+    if (!inbound.enabled) {
+      return { ...inbound, enabled: false };
+    }
+    const targetHost = inbound.targetHost?.trim();
+    const targetPort = Number(inbound.targetPort);
+    if (!targetHost) throw new Error('inbound.targetHost is required when inbound routing is enabled');
+    if (!Number.isInteger(targetPort) || targetPort < 1 || targetPort > 65535) {
+      throw new Error(`Invalid inbound.targetPort: ${inbound.targetPort}`);
+    }
+    return {
+      ...inbound,
+      targetHost,
+      targetPort,
+    };
+  }
+
+  private matchesOwnership(
+    ownership: interfaces.data.IWorkAppMailOwnership,
+    filter?: Partial<interfaces.data.IWorkAppMailOwnership>,
+  ): boolean {
+    if (!filter) return true;
+    if (filter.workHosterType && filter.workHosterType !== ownership.workHosterType) return false;
+    if (filter.workHosterId && filter.workHosterId !== ownership.workHosterId) return false;
+    if (filter.workAppId && filter.workAppId !== ownership.workAppId) return false;
+    return true;
+  }
+
+  private buildExternalKey(
+    ownership: interfaces.data.IWorkAppMailOwnership,
+    address: string,
+  ): string {
+    return [
+      ownership.workHosterType,
+      ownership.workHosterId,
+      ownership.workAppId,
+      address,
+    ].join(':');
+  }
+
+  private buildSmtpUsername(externalKey: string): string {
+    return `workapp-${this.hashExternalKey(externalKey).slice(0, 24)}`;
+  }
+
+  private buildRouteName(externalKey: string): string {
+    return `workapp-mail-${this.hashExternalKey(externalKey).slice(0, 32)}`;
+  }
+
+  private hashExternalKey(externalKey: string): string {
+    return plugins.crypto.createHash('sha256').update(externalKey).digest('hex');
+  }
+
+  private generateSmtpPassword(): string {
+    return plugins.crypto.randomBytes(24).toString('base64url');
+  }
+
+  private isManagedMailRouteName(routeName: string): boolean {
+    return routeName.startsWith('workapp-mail-');
+  }
+
+  private isManagedSmtpUsername(username: string): boolean {
+    return username.startsWith('workapp-');
+  }
+
+  private buildSmtpCredentials(
+    identity: IStoredWorkAppMailIdentity,
+  ): interfaces.data.IWorkAppMailCredentials {
+    return {
+      username: identity.smtp.username,
+      password: identity.smtpPassword,
+      host: this.dcRouterRef.options.emailConfig?.outbound?.hostname
+        || this.dcRouterRef.options.emailConfig?.hostname,
+      ports: {
+        smtp: this.dcRouterRef.options.emailConfig?.ports?.includes(25) ? 25 : undefined,
+        submission: this.dcRouterRef.options.emailConfig?.ports?.includes(587) ? 587 : undefined,
+        smtps: this.dcRouterRef.options.emailConfig?.ports?.includes(465) ? 465 : undefined,
+      },
+    };
+  }
+
+  private toPublicIdentity(
+    identity: IStoredWorkAppMailIdentity,
+  ): interfaces.data.IWorkAppMailIdentity {
+    const { smtpPassword, ...publicIdentity } = identity;
+    return publicIdentity;
+  }
+}
diff --git a/ts/email/index.ts b/ts/email/index.ts
index 24d399c..2aa0edc 100644
--- a/ts/email/index.ts
+++ b/ts/email/index.ts
@@ -1,3 +1,4 @@
 export * from './classes.email-domain.manager.js';
 export * from './classes.smartmta-storage-manager.js';
+export * from './classes.workapp-mail-manager.js';
 export * from './email-dns-records.js';
diff --git a/ts/opsserver/handlers/workhoster.handler.ts b/ts/opsserver/handlers/workhoster.handler.ts
index dfb2cdc..486a158 100644
--- a/ts/opsserver/handlers/workhoster.handler.ts
+++ b/ts/opsserver/handlers/workhoster.handler.ts
@@ -129,6 +129,36 @@ export class WorkHosterHandler {
         },
       ),
     );
+
+    this.typedrouter.addTypedHandler(
+      new plugins.typedrequest.TypedHandler<interfaces.requests.IReq_GetWorkAppMailIdentities>(
+        'getWorkAppMailIdentities',
+        async (dataArg) => {
+          await this.requireAuth(dataArg, 'workhosters:read');
+          const manager = this.opsServerRef.dcRouterRef.workAppMailManager;
+          if (!manager) return { identities: [] };
+          return { identities: await manager.listMailIdentities(dataArg.ownership) };
+        },
+      ),
+    );
+
+    this.typedrouter.addTypedHandler(
+      new plugins.typedrequest.TypedHandler<interfaces.requests.IReq_SyncWorkAppMailIdentity>(
+        'syncWorkAppMailIdentity',
+        async (dataArg) => {
+          const userId = await this.requireAuth(dataArg, 'workhosters:write');
+          const manager = this.opsServerRef.dcRouterRef.workAppMailManager;
+          if (!manager) {
+            return { success: false, message: 'WorkApp mail manager not initialized' };
+          }
+          try {
+            return await manager.syncMailIdentity(dataArg, userId);
+          } catch (error) {
+            return { success: false, message: (error as Error).message };
+          }
+        },
+      ),
+    );
   }
 
   private getGatewayCapabilities(): interfaces.data.IGatewayCapabilities {
diff --git a/ts_interfaces/data/workhoster.ts b/ts_interfaces/data/workhoster.ts
index b7f5c52..90e1418 100644
--- a/ts_interfaces/data/workhoster.ts
+++ b/ts_interfaces/data/workhoster.ts
@@ -54,3 +54,55 @@ export interface IWorkAppRouteSyncResult {
   routeId?: string;
   message?: string;
 }
+
+export interface IWorkAppMailOwnership {
+  workHosterType: 'onebox' | 'cloudly' | 'custom';
+  workHosterId: string;
+  workAppId: string;
+}
+
+export interface IWorkAppMailInboundRoute {
+  enabled: boolean;
+  targetHost: string;
+  targetPort: number;
+  preserveHeaders?: boolean;
+  addHeaders?: Record<string, string>;
+}
+
+export interface IWorkAppMailIdentity {
+  id: string;
+  externalKey: string;
+  ownership: IWorkAppMailOwnership;
+  address: string;
+  localPart: string;
+  domain: string;
+  enabled: boolean;
+  displayName?: string;
+  inbound?: IWorkAppMailInboundRoute;
+  smtp: {
+    enabled: boolean;
+    username: string;
+  };
+  createdAt: number;
+  updatedAt: number;
+  createdBy: string;
+}
+
+export interface IWorkAppMailCredentials {
+  username: string;
+  password: string;
+  host?: string;
+  ports?: {
+    smtp?: number;
+    submission?: number;
+    smtps?: number;
+  };
+}
+
+export interface IWorkAppMailIdentitySyncResult {
+  success: boolean;
+  action?: 'created' | 'updated' | 'deleted' | 'unchanged';
+  identity?: IWorkAppMailIdentity;
+  smtpCredentials?: IWorkAppMailCredentials;
+  message?: string;
+}
diff --git a/ts_interfaces/requests/workhoster.ts b/ts_interfaces/requests/workhoster.ts
index bb1d07e..95dbfbc 100644
--- a/ts_interfaces/requests/workhoster.ts
+++ b/ts_interfaces/requests/workhoster.ts
@@ -2,6 +2,10 @@ import * as plugins from '../plugins.js';
 import type * as authInterfaces from '../data/auth.js';
 import type {
   IGatewayCapabilities,
+  IWorkAppMailIdentity,
+  IWorkAppMailIdentitySyncResult,
+  IWorkAppMailInboundRoute,
+  IWorkAppMailOwnership,
   IWorkAppRouteOwnership,
   IWorkAppRouteSyncResult,
   IWorkHosterDomain,
@@ -51,3 +55,39 @@ export interface IReq_SyncWorkAppRoute extends plugins.typedrequestInterfaces.im
   };
   response: IWorkAppRouteSyncResult;
 }
+
+export interface IReq_GetWorkAppMailIdentities extends plugins.typedrequestInterfaces.implementsTR<
+  plugins.typedrequestInterfaces.ITypedRequest,
+  IReq_GetWorkAppMailIdentities
+> {
+  method: 'getWorkAppMailIdentities';
+  request: {
+    identity?: authInterfaces.IIdentity;
+    apiToken?: string;
+    ownership?: Partial<IWorkAppMailOwnership>;
+  };
+  response: {
+    identities: IWorkAppMailIdentity[];
+  };
+}
+
+export interface IReq_SyncWorkAppMailIdentity extends plugins.typedrequestInterfaces.implementsTR<
+  plugins.typedrequestInterfaces.ITypedRequest,
+  IReq_SyncWorkAppMailIdentity
+> {
+  method: 'syncWorkAppMailIdentity';
+  request: {
+    identity?: authInterfaces.IIdentity;
+    apiToken?: string;
+    ownership: IWorkAppMailOwnership;
+    localPart: string;
+    domain: string;
+    displayName?: string;
+    inbound?: IWorkAppMailInboundRoute;
+    enabled?: boolean;
+    smtpEnabled?: boolean;
+    resetSmtpPassword?: boolean;
+    delete?: boolean;
+  };
+  response: IWorkAppMailIdentitySyncResult;
+}