diff --git a/.changelog/NEXT.md b/.changelog/NEXT.md
index 64db6f7b..88bfb297 100644
--- a/.changelog/NEXT.md
+++ b/.changelog/NEXT.md
@@ -50,6 +50,7 @@
 
 ## Fixed
 
+- **[issue-158] Unknown API routes now return JSON errors** — Requests to unrecognized `/api` paths receive a stable 404 error envelope instead of the browser app's HTML, while client-side navigation continues to use the SPA fallback.
 - Search results now keep their alphabetical ordering. The batch person-loader (`getPersonsBatch`) re-orders rows back to the requested order, fixing a regression where SQLite's `WHERE person_id IN (...)` returned rows in table order and silently discarded the search query's `ORDER BY display_name` (so the default, unsorted search view appeared randomly ordered).
 - Platform comparison now treats equivalent place spellings as matches: "Dallas, Texas, USA" vs "Dallas, Texas, United States" (and U.S.A. / United States of America / state abbreviations like TX vs Texas, UK vs United Kingdom, etc.) — no longer flagged as `different`. Place containment is now suffix-based, so "Texas" no longer falsely matches "Texarkana"
 - Platform comparison now treats equivalent date formats as matches (e.g., "1979-07-31" vs "31 JUL 1979")
diff --git a/docs/api.md b/docs/api.md
index b476efcd..d14d0779 100644
--- a/docs/api.md
+++ b/docs/api.md
@@ -1,6 +1,6 @@
 # API Reference
 
-Backend runs on port 6374 by default. All endpoints return JSON with `{ success: boolean, data?: T, error?: string }`.
+Backend runs on port 6374 by default. Application JSON endpoints use the envelope `{ success: boolean, data?: T, error?: string }`. Explicitly documented file downloads and server-sent event (SSE) streams retain their native payloads, while `/api/health` returns its operational status object directly. Requests that do not match an `/api` endpoint return HTTP 404 with `{ success: false, error: "API route not found" }`.
 
 ## Databases (Roots)
 
diff --git a/server/src/app.ts b/server/src/app.ts
new file mode 100644
index 00000000..33defc9d
--- /dev/null
+++ b/server/src/app.ts
@@ -0,0 +1,112 @@
+import cors from 'cors';
+import express, { type Express } from 'express';
+import { existsSync } from 'fs';
+import path from 'path';
+import { fileURLToPath } from 'url';
+import { apiNotFound } from './middleware/apiNotFound.js';
+import { errorHandler } from './middleware/errorHandler.js';
+import { requestLogger } from './middleware/requestLogger.js';
+import { requestTimeout } from './middleware/requestTimeout.js';
+import { aiDiscoveryRouter } from './routes/ai-discovery.routes.js';
+import { ancestryHintsRouter } from './routes/ancestry-hints.routes.js';
+import { ancestryTreeRouter } from './routes/ancestry-tree.routes.js';
+import { ancestryUpdateRouter } from './routes/ancestry-update.routes.js';
+import { auditorRouter } from './routes/auditor.routes.js';
+import { augmentationRouter } from './routes/augmentation.routes.js';
+import { browserRouter } from './routes/browser.routes.js';
+import { databaseRoutes } from './routes/database.routes.js';
+import { deathsRouter } from './routes/deaths.routes.js';
+import { exportRoutes } from './routes/export.routes.js';
+import { favoritesRouter } from './routes/favorites.routes.js';
+import { gedcomRouter } from './routes/gedcom.routes.js';
+import { genealogyProviderRouter } from './routes/genealogy-provider.routes.js';
+import { indexerRoutes } from './routes/indexer.routes.js';
+import { integrityRouter } from './routes/integrity.routes.js';
+import { mapRouter } from './routes/map.routes.js';
+import { pathRoutes } from './routes/path.routes.js';
+import { personRoutes } from './routes/person.routes.js';
+import { providerRouter } from './routes/provider.routes.js';
+import { searchRoutes } from './routes/search.routes.js';
+import { syncRouter } from './routes/sync.routes.js';
+import { testRunnerRouter } from './routes/test-runner.routes.js';
+import { initAIToolkit } from './services/ai-toolkit.service.js';
+import { logger } from './lib/logger.js';
+
+const CORS_ORIGIN = process.env.CORS_ORIGIN || 'http://localhost:6373';
+const corsOrigin = CORS_ORIGIN.includes(',')
+  ? CORS_ORIGIN.split(',').map(origin => {
+      const trimmed = origin.trim();
+      new URL(trimmed);
+      return trimmed;
+    })
+  : CORS_ORIGIN;
+
+const __dirname = path.dirname(fileURLToPath(import.meta.url));
+const CLIENT_DIST = path.join(__dirname, '..', '..', 'client', 'dist');
+const CLIENT_DIST_ALT = path.join(__dirname, '..', '..', '..', 'client', 'dist');
+
+const findClientDist = (): string => (
+  existsSync(CLIENT_DIST) ? CLIENT_DIST : CLIENT_DIST_ALT
+);
+
+export interface CreateAppOptions {
+  aiToolkit?: {
+    mountRoutes: (app: Express) => void;
+  };
+  clientDist?: string;
+}
+
+export const createApp = ({
+  aiToolkit = initAIToolkit(null),
+  clientDist = findClientDist()
+}: CreateAppOptions = {}): Express => {
+  const app = express();
+
+  app.use(cors({ origin: corsOrigin }));
+  app.use(express.json());
+  app.use(requestTimeout);
+  app.use(requestLogger);
+
+  aiToolkit.mountRoutes(app);
+
+  app.use('/api/databases', databaseRoutes);
+  app.use('/api/persons', personRoutes);
+  app.use('/api/search', searchRoutes);
+  app.use('/api/path', pathRoutes);
+  app.use('/api/indexer', indexerRoutes);
+  app.use('/api/export', exportRoutes);
+  app.use('/api/browser', browserRouter);
+  app.use('/api/augment', augmentationRouter);
+  app.use('/api/genealogy-providers', genealogyProviderRouter);
+  app.use('/api/scrape-providers', providerRouter);
+  app.use('/api/gedcom', gedcomRouter);
+  app.use('/api/sync', syncRouter);
+  app.use('/api/favorites', favoritesRouter);
+  app.use('/api/ancestry-tree', ancestryTreeRouter);
+  app.use('/api/ai-discovery', aiDiscoveryRouter);
+  app.use('/api/test-runner', testRunnerRouter);
+  app.use('/api/integrity', integrityRouter);
+  app.use('/api/ancestry-hints', ancestryHintsRouter);
+  app.use('/api/ancestry-update', ancestryUpdateRouter);
+  app.use('/api/map', mapRouter);
+  app.use('/api/audit', auditorRouter);
+  app.use('/api/deaths', deathsRouter);
+
+  app.get('/api/health', (_req, res) => {
+    res.json({ status: 'ok', timestamp: new Date().toISOString() });
+  });
+
+  app.use('/api', apiNotFound);
+
+  if (existsSync(clientDist)) {
+    app.use(express.static(clientDist));
+    app.get('/{*splat}', (_req, res) => {
+      res.sendFile(path.join(clientDist, 'index.html'));
+    });
+    logger.ok('server', 'Serving built UI from client/dist');
+  }
+
+  app.use(errorHandler);
+
+  return app;
+};
diff --git a/server/src/index.ts b/server/src/index.ts
index 6ae92efb..64311c18 100644
--- a/server/src/index.ts
+++ b/server/src/index.ts
@@ -1,112 +1,14 @@
-import express from 'express';
-import cors from 'cors';
-import { existsSync } from 'fs';
 import { createServer } from 'http';
-import path from 'path';
-import { fileURLToPath } from 'url';
-import { initAIToolkit } from './services/ai-toolkit.service.js';
-import { databaseRoutes } from './routes/database.routes.js';
-import { personRoutes } from './routes/person.routes.js';
-import { searchRoutes } from './routes/search.routes.js';
-import { pathRoutes } from './routes/path.routes.js';
-import { indexerRoutes } from './routes/indexer.routes.js';
-import { exportRoutes } from './routes/export.routes.js';
-import { browserRouter } from './routes/browser.routes.js';
 import { browserService } from './services/browser.service.js';
-import { augmentationRouter } from './routes/augmentation.routes.js';
-import { genealogyProviderRouter } from './routes/genealogy-provider.routes.js';
-import { providerRouter } from './routes/provider.routes.js';
-import { gedcomRouter } from './routes/gedcom.routes.js';
-import { syncRouter } from './routes/sync.routes.js';
-import { favoritesRouter } from './routes/favorites.routes.js';
-import { ancestryTreeRouter } from './routes/ancestry-tree.routes.js';
-import { aiDiscoveryRouter } from './routes/ai-discovery.routes.js';
-import { testRunnerRouter } from './routes/test-runner.routes.js';
-import { integrityRouter } from './routes/integrity.routes.js';
-import { ancestryHintsRouter } from './routes/ancestry-hints.routes.js';
-import { ancestryUpdateRouter } from './routes/ancestry-update.routes.js';
-import { mapRouter } from './routes/map.routes.js';
-import { auditorRouter } from './routes/auditor.routes.js';
-import { deathsRouter } from './routes/deaths.routes.js';
 import { runMigrations } from './db/migrations/index.js';
-import { errorHandler } from './middleware/errorHandler.js';
-import { requestLogger } from './middleware/requestLogger.js';
-import { requestTimeout } from './middleware/requestTimeout.js';
 import { logger } from './lib/logger.js';
+import { createApp } from './app.js';
 
-const CORS_ORIGIN = process.env.CORS_ORIGIN || 'http://localhost:6373';
-const corsOrigin = CORS_ORIGIN.includes(',')
-  ? CORS_ORIGIN.split(',').map(o => {
-      const trimmed = o.trim();
-      new URL(trimmed); // throws on invalid origin
-      return trimmed;
-    })
-  : CORS_ORIGIN;
-
-const app = express();
+const app = createApp();
 const httpServer = createServer(app);
 
 const PORT = parseInt(process.env.PORT || '6374', 10);
 
-// Middleware
-app.use(cors({ origin: corsOrigin }));
-app.use(express.json());
-app.use(requestTimeout);
-app.use(requestLogger);
-
-// Initialize AI Toolkit with routes for providers, runs, and prompts
-const aiToolkit = initAIToolkit(null);
-aiToolkit.mountRoutes(app);
-
-// Routes
-app.use('/api/databases', databaseRoutes);
-app.use('/api/persons', personRoutes);
-app.use('/api/search', searchRoutes);
-app.use('/api/path', pathRoutes);
-app.use('/api/indexer', indexerRoutes);
-app.use('/api/export', exportRoutes);
-app.use('/api/browser', browserRouter);
-app.use('/api/augment', augmentationRouter);
-app.use('/api/genealogy-providers', genealogyProviderRouter);
-app.use('/api/scrape-providers', providerRouter);
-app.use('/api/gedcom', gedcomRouter);
-app.use('/api/sync', syncRouter);
-app.use('/api/favorites', favoritesRouter);
-app.use('/api/ancestry-tree', ancestryTreeRouter);
-app.use('/api/ai-discovery', aiDiscoveryRouter);
-app.use('/api/test-runner', testRunnerRouter);
-app.use('/api/integrity', integrityRouter);
-app.use('/api/ancestry-hints', ancestryHintsRouter);
-app.use('/api/ancestry-update', ancestryUpdateRouter);
-app.use('/api/map', mapRouter);
-app.use('/api/audit', auditorRouter);
-app.use('/api/deaths', deathsRouter);
-
-// Health check
-app.get('/api/health', (_req, res) => {
-  res.json({ status: 'ok', timestamp: new Date().toISOString() });
-});
-
-// Serve built client UI in production
-const __filename = fileURLToPath(import.meta.url);
-const __dirname = path.dirname(__filename);
-// From src/index.ts: up to server/, then to project root, then client/dist
-const CLIENT_DIST = path.join(__dirname, '..', '..', 'client', 'dist');
-// From dist/index.js (compiled): up to server/, then to project root, then client/dist
-const CLIENT_DIST_ALT = path.join(__dirname, '..', '..', '..', 'client', 'dist');
-const clientDist = existsSync(CLIENT_DIST) ? CLIENT_DIST : CLIENT_DIST_ALT;
-
-if (existsSync(clientDist)) {
-  app.use(express.static(clientDist));
-  app.get('/{*splat}', (_req, res) => {
-    res.sendFile(path.join(clientDist, 'index.html'));
-  });
-  logger.ok('server', 'Serving built UI from client/dist');
-}
-
-// Error handling
-app.use(errorHandler);
-
 const HOST = process.env.HOST || 'localhost';
 
 const shutdown = () => {
diff --git a/server/src/middleware/apiNotFound.ts b/server/src/middleware/apiNotFound.ts
new file mode 100644
index 00000000..323ea30f
--- /dev/null
+++ b/server/src/middleware/apiNotFound.ts
@@ -0,0 +1,8 @@
+import type { RequestHandler } from 'express';
+
+export const apiNotFound: RequestHandler = (_req, res) => {
+  res.status(404).json({
+    success: false,
+    error: 'API route not found'
+  });
+};
diff --git a/tests/integration/api/notFound.spec.ts b/tests/integration/api/notFound.spec.ts
new file mode 100644
index 00000000..70d68a09
--- /dev/null
+++ b/tests/integration/api/notFound.spec.ts
@@ -0,0 +1,56 @@
+import { mkdtempSync, rmSync, writeFileSync } from 'fs';
+import { tmpdir } from 'os';
+import path from 'path';
+import type { Express } from 'express';
+import request from 'supertest';
+import { afterAll, beforeAll, describe, expect, it } from 'vitest';
+import { createApp } from '../../../server/src/app.js';
+
+describe('terminal API boundary', () => {
+  let app: Express;
+  let clientDist: string;
+
+  beforeAll(() => {
+    clientDist = mkdtempSync(path.join(tmpdir(), 'sparsetree-client-'));
+    writeFileSync(
+      path.join(clientDist, 'index.html'),
+      '<!doctype html><html><body>SparseTree test client</body></html>'
+    );
+    app = createApp({
+      aiToolkit: { mountRoutes: () => undefined },
+      clientDist
+    });
+  });
+
+  afterAll(() => {
+    rmSync(clientDist, { recursive: true, force: true });
+  });
+
+  it.each([
+    ['get', '/api/persons/missing/typo/extra'],
+    ['post', '/api/missing']
+  ] as const)('returns the JSON error envelope for unknown %s routes', async (method, url) => {
+    const response = await request(app)[method](url).expect(404);
+
+    expect(response.type).toBe('application/json');
+    expect(response.body).toEqual({
+      success: false,
+      error: 'API route not found'
+    });
+  });
+
+  it('keeps registered API routes ahead of the terminal boundary', async () => {
+    const response = await request(app).get('/api/health').expect(200);
+
+    expect(response.body.status).toBe('ok');
+  });
+
+  it('keeps non-API navigation behind the SPA fallback', async () => {
+    const response = await request(app)
+      .get('/people/interesting-ancestor')
+      .expect(200);
+
+    expect(response.type).toBe('text/html');
+    expect(response.text).toContain('SparseTree test client');
+  });
+});