diff --git a/apps/desktop/electron/dashboard-token.cjs b/apps/desktop/electron/dashboard-token.cjs
new file mode 100644
index 00000000000..12f1dd400d3
--- /dev/null
+++ b/apps/desktop/electron/dashboard-token.cjs
@@ -0,0 +1,87 @@
+/**
+ * Helpers for local dashboard session-token discovery.
+ *
+ * The desktop main process can pass HERMES_DASHBOARD_SESSION_TOKEN when it
+ * spawns the local dashboard, but the dashboard is the source of truth for the
+ * token it actually serves to the renderer. If those drift, HTTP readiness
+ * probes still pass while /api/ws rejects the renderer's token.
+ */
+
+const http = require('node:http')
+const https = require('node:https')
+
+const DEFAULT_TOKEN_FETCH_TIMEOUT_MS = 3_000
+
+function fetchPublicText(url, options = {}) {
+  return new Promise((resolve, reject) => {
+    let parsed
+    try {
+      parsed = new URL(url)
+    } catch (error) {
+      reject(new Error(`Invalid URL: ${error.message}`))
+      return
+    }
+
+    if (parsed.protocol !== 'http:' && parsed.protocol !== 'https:') {
+      reject(new Error(`Unsupported Hermes backend URL protocol: ${parsed.protocol}`))
+      return
+    }
+
+    const client = parsed.protocol === 'https:' ? https : http
+    const timeoutMs = options.timeoutMs ?? DEFAULT_TOKEN_FETCH_TIMEOUT_MS
+    const req = client.request(parsed, { method: options.method || 'GET' }, res => {
+      const chunks = []
+      res.on('data', chunk => chunks.push(chunk))
+      res.on('end', () => {
+        const text = Buffer.concat(chunks).toString('utf8')
+        if ((res.statusCode || 500) >= 400) {
+          reject(new Error(`${res.statusCode}: ${text || res.statusMessage}`))
+          return
+        }
+        resolve(text)
+      })
+    })
+
+    req.on('error', reject)
+    req.setTimeout(timeoutMs, () => {
+      req.destroy(new Error(`Timed out connecting to Hermes backend after ${timeoutMs}ms`))
+    })
+    req.end()
+  })
+}
+
+function extractInjectedDashboardToken(html) {
+  const match = /window\.__HERMES_SESSION_TOKEN__\s*=\s*("(?:\\.|[^"\\])*")/.exec(String(html || ''))
+  if (!match) return null
+  try {
+    return JSON.parse(match[1])
+  } catch {
+    return null
+  }
+}
+
+function dashboardIndexUrl(baseUrl) {
+  return `${String(baseUrl || '').replace(/\/+$/, '')}/`
+}
+
+async function resolveServedDashboardToken(baseUrl, fallbackToken, options = {}) {
+  const fetchText = options.fetchText || fetchPublicText
+  const html = await fetchText(dashboardIndexUrl(baseUrl), {
+    timeoutMs: options.timeoutMs ?? DEFAULT_TOKEN_FETCH_TIMEOUT_MS
+  })
+  const servedToken = extractInjectedDashboardToken(html)
+
+  if (servedToken && servedToken !== fallbackToken && typeof options.rememberLog === 'function') {
+    options.rememberLog('[boot] dashboard served a different session token; using served token for WebSocket auth')
+  }
+
+  return servedToken || fallbackToken
+}
+
+module.exports = {
+  DEFAULT_TOKEN_FETCH_TIMEOUT_MS,
+  dashboardIndexUrl,
+  extractInjectedDashboardToken,
+  fetchPublicText,
+  resolveServedDashboardToken
+}
diff --git a/apps/desktop/electron/dashboard-token.test.cjs b/apps/desktop/electron/dashboard-token.test.cjs
new file mode 100644
index 00000000000..2a7e05c4fed
--- /dev/null
+++ b/apps/desktop/electron/dashboard-token.test.cjs
@@ -0,0 +1,89 @@
+/**
+ * Tests for electron/dashboard-token.cjs.
+ *
+ * Run with: node --test electron/dashboard-token.test.cjs
+ * (Wired into npm test:desktop:platforms in package.json.)
+ */
+
+const test = require('node:test')
+const assert = require('node:assert/strict')
+
+const {
+  dashboardIndexUrl,
+  extractInjectedDashboardToken,
+  fetchPublicText,
+  resolveServedDashboardToken
+} = require('./dashboard-token.cjs')
+
+test('extractInjectedDashboardToken reads the JSON-encoded dashboard token', () => {
+  const html = '<script>window.__HERMES_SESSION_TOKEN__="served-token";window.__HERMES_BASE_PATH__=""</script>'
+  assert.equal(extractInjectedDashboardToken(html), 'served-token')
+})
+
+test('extractInjectedDashboardToken handles escaped token strings', () => {
+  const html = '<script>window.__HERMES_SESSION_TOKEN__="served\\\\token\\"quoted";</script>'
+  assert.equal(extractInjectedDashboardToken(html), 'served\\token"quoted')
+})
+
+test('extractInjectedDashboardToken returns null for missing or malformed values', () => {
+  assert.equal(extractInjectedDashboardToken('<html></html>'), null)
+  assert.equal(extractInjectedDashboardToken('<script>window.__HERMES_SESSION_TOKEN__={bad}</script>'), null)
+})
+
+test('dashboardIndexUrl preserves dashboard path prefixes', () => {
+  assert.equal(dashboardIndexUrl('http://127.0.0.1:9120'), 'http://127.0.0.1:9120/')
+  assert.equal(dashboardIndexUrl('https://host.example/hermes/'), 'https://host.example/hermes/')
+})
+
+test('resolveServedDashboardToken uses the served token and logs when it differs', async () => {
+  const logs = []
+  const token = await resolveServedDashboardToken('http://127.0.0.1:9120', 'spawn-token', {
+    fetchText: async url => {
+      assert.equal(url, 'http://127.0.0.1:9120/')
+      return '<script>window.__HERMES_SESSION_TOKEN__="served-token";</script>'
+    },
+    rememberLog: line => logs.push(line)
+  })
+
+  assert.equal(token, 'served-token')
+  assert.equal(logs.length, 1)
+  assert.match(logs[0], /served a different session token/)
+})
+
+test('resolveServedDashboardToken falls back when the served HTML has no token', async () => {
+  const token = await resolveServedDashboardToken('http://127.0.0.1:9120', 'spawn-token', {
+    fetchText: async () => '<html></html>',
+    rememberLog: () => {
+      throw new Error('should not log when no served token is present')
+    }
+  })
+
+  assert.equal(token, 'spawn-token')
+})
+
+test('resolveServedDashboardToken does not log when served token matches fallback', async () => {
+  const token = await resolveServedDashboardToken('http://127.0.0.1:9120', 'same-token', {
+    fetchText: async () => '<script>window.__HERMES_SESSION_TOKEN__="same-token";</script>',
+    rememberLog: () => {
+      throw new Error('should not log when token already matches')
+    }
+  })
+
+  assert.equal(token, 'same-token')
+})
+
+test('resolveServedDashboardToken propagates fetch errors so callers can fall back explicitly', async () => {
+  await assert.rejects(
+    () =>
+      resolveServedDashboardToken('http://127.0.0.1:9120', 'spawn-token', {
+        fetchText: async () => {
+          throw new Error('boom')
+        }
+      }),
+    /boom/
+  )
+})
+
+test('fetchPublicText rejects unsupported protocols', async () => {
+  await assert.rejects(() => fetchPublicText('file:///tmp/index.html'), /Unsupported Hermes backend URL protocol/)
+})
diff --git a/apps/desktop/electron/main.cjs b/apps/desktop/electron/main.cjs
index bfa5e178d2f..2c6aa425cf2 100644
--- a/apps/desktop/electron/main.cjs
+++ b/apps/desktop/electron/main.cjs
@@ -29,6 +29,7 @@ const { runBootstrap } = require('./bootstrap-runner.cjs')
 const { buildSessionWindowUrl, createSessionWindowRegistry } = require('./session-windows.cjs')
 const { canImportHermesCli, verifyHermesCli } = require('./backend-probes.cjs')
 const { probeGatewayWebSocket } = require('./gateway-ws-probe.cjs')
+const { resolveServedDashboardToken } = require('./dashboard-token.cjs')
 const { serializeJsonBody, setJsonRequestHeaders } = require('./oauth-net-request.cjs')
 const { fetchMarketplaceThemes, searchMarketplaceThemes } = require('./vscode-marketplace.cjs')
 const { readDirForIpc } = require('./fs-read-dir.cjs')
@@ -4594,15 +4595,20 @@ async function spawnPoolBackend(profile, entry) {
   const baseUrl = `http://127.0.0.1:${port}`
   await Promise.race([waitForHermes(baseUrl, token), startFailed])
   ready = true
+  const authToken = await resolveServedDashboardToken(baseUrl, token, { rememberLog }).catch(error => {
+    rememberLog(`[boot] could not read served dashboard token for profile "${profile}": ${error.message}`)
+    return token
+  })
+  entry.token = authToken
 
   return {
     baseUrl,
     mode: 'local',
     source: 'local',
     authMode: 'token',
-    token,
+    token: authToken,
     profile,
-    wsUrl: `ws://127.0.0.1:${port}/api/ws?token=${encodeURIComponent(token)}`,
+    wsUrl: `ws://127.0.0.1:${port}/api/ws?token=${encodeURIComponent(authToken)}`,
     logs: hermesLog.slice(-80),
     ...getWindowState()
   }
@@ -4821,6 +4827,10 @@ async function startHermes() {
     await advanceBootProgress('backend.wait', 'Waiting for Hermes backend to become ready', 90)
     await Promise.race([waitForHermes(baseUrl, token), backendStartFailed])
     backendReady = true
+    const authToken = await resolveServedDashboardToken(baseUrl, token, { rememberLog }).catch(error => {
+      rememberLog(`[boot] could not read served dashboard token: ${error.message}`)
+      return token
+    })
     updateBootProgress({
       phase: 'backend.ready',
       message: 'Hermes backend is ready. Finalizing desktop startup',
@@ -4834,8 +4844,8 @@ async function startHermes() {
       mode: 'local',
       source: 'local',
       authMode: 'token',
-      token,
-      wsUrl: `ws://127.0.0.1:${port}/api/ws?token=${encodeURIComponent(token)}`,
+      token: authToken,
+      wsUrl: `ws://127.0.0.1:${port}/api/ws?token=${encodeURIComponent(authToken)}`,
       logs: hermesLog.slice(-80),
       ...getWindowState()
     }
diff --git a/apps/desktop/electron/windows-child-process.test.cjs b/apps/desktop/electron/windows-child-process.test.cjs
index 6bcc58a0a33..92989c978bb 100644
--- a/apps/desktop/electron/windows-child-process.test.cjs
+++ b/apps/desktop/electron/windows-child-process.test.cjs
@@ -8,7 +8,7 @@ const path = require('node:path')
 const ELECTRON_DIR = __dirname
 
 function readElectronFile(name) {
-  return fs.readFileSync(path.join(ELECTRON_DIR, name), 'utf8')
+  return fs.readFileSync(path.join(ELECTRON_DIR, name), 'utf8').replace(/\r\n/g, '\n')
 }
 
 function requireHiddenChildOptions(source, needle) {
diff --git a/apps/desktop/package.json b/apps/desktop/package.json
index d247476ebeb..6d2e1b0ce1c 100644
--- a/apps/desktop/package.json
+++ b/apps/desktop/package.json
@@ -35,7 +35,7 @@
     "test:desktop:nsis": "node scripts/test-desktop.mjs nsis",
     "test:desktop:existing": "node scripts/test-desktop.mjs existing",
     "test:desktop:fresh": "node scripts/test-desktop.mjs fresh",
-    "test:desktop:platforms": "node --test electron/bootstrap-platform.test.cjs electron/hardening.test.cjs electron/backend-probes.test.cjs electron/bootstrap-runner.test.cjs electron/connection-config.test.cjs electron/gateway-ws-probe.test.cjs electron/oauth-net-request.test.cjs electron/desktop-uninstall.test.cjs electron/session-windows.test.cjs electron/workspace-cwd.test.cjs electron/fs-read-dir.test.cjs electron/git-root.test.cjs electron/windows-child-process.test.cjs electron/update-remote.test.cjs",
+    "test:desktop:platforms": "node --test electron/bootstrap-platform.test.cjs electron/hardening.test.cjs electron/backend-probes.test.cjs electron/bootstrap-runner.test.cjs electron/connection-config.test.cjs electron/dashboard-token.test.cjs electron/gateway-ws-probe.test.cjs electron/oauth-net-request.test.cjs electron/desktop-uninstall.test.cjs electron/session-windows.test.cjs electron/workspace-cwd.test.cjs electron/fs-read-dir.test.cjs electron/git-root.test.cjs electron/windows-child-process.test.cjs electron/update-remote.test.cjs",
     "typecheck": "tsc -p . --noEmit",
     "lint": "eslint src/ electron/",
     "lint:fix": "eslint src/ electron/ --fix",