diff --git a/src/main/azure-devops/azure-devops-api-request.test.ts b/src/main/azure-devops/azure-devops-api-request.test.ts
new file mode 100644
index 00000000000..a804ebcadb0
--- /dev/null
+++ b/src/main/azure-devops/azure-devops-api-request.test.ts
@@ -0,0 +1,134 @@
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
+import {
+  _resetAzureDevOpsPreviewApiVersionCache,
+  requestAzureDevOpsJson,
+  requestAzureDevOpsJsonAtBase
+} from './azure-devops-api-request'
+import type { AzureDevOpsRepoRef } from './repository-ref'
+
+const OLD_ENV = process.env
+const OLD_FETCH = globalThis.fetch
+
+const SERVER_BASE = 'https://ado.example.com:8443/tfs/MyCollection'
+
+function previewRejection(): Response {
+  return new Response(
+    JSON.stringify({
+      message:
+        'The requested version "7.1" of the resource is under preview. The -preview flag must be supplied in the api-version for such requests. For example: "7.1-preview"',
+      typeKey: 'VssInvalidPreviewVersionException'
+    }),
+    { status: 400, headers: { 'Content-Type': 'application/json' } }
+  )
+}
+
+function serverRepoRef(): AzureDevOpsRepoRef {
+  return {
+    host: 'ado.example.com',
+    organization: null,
+    project: 'MyProject',
+    repository: 'my-repo',
+    apiBaseUrl: `${SERVER_BASE}/MyProject`,
+    webBaseUrl: `${SERVER_BASE}/MyProject/_git/my-repo`
+  }
+}
+
+describe('Azure DevOps API request (STA-3494)', () => {
+  beforeEach(() => {
+    process.env = { ...OLD_ENV, ORCA_AZURE_DEVOPS_TOKEN: 'pat-token' }
+    delete process.env.ORCA_AZURE_DEVOPS_API_BASE_URL
+    _resetAzureDevOpsPreviewApiVersionCache()
+  })
+
+  afterEach(() => {
+    process.env = OLD_ENV
+    globalThis.fetch = OLD_FETCH
+  })
+
+  it('retries with -preview when Azure DevOps Server rejects the api-version', async () => {
+    const versions: (string | null)[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      const url = new URL(String(input))
+      versions.push(url.searchParams.get('api-version'))
+      if (!url.searchParams.get('api-version')?.endsWith('-preview')) {
+        return previewRejection()
+      }
+      return Response.json({ authenticatedUser: { providerDisplayName: 'Server User' } })
+    }) as never
+
+    await expect(
+      requestAzureDevOpsJsonAtBase(SERVER_BASE, '/_apis/connectionData')
+    ).resolves.toEqual({ authenticatedUser: { providerDisplayName: 'Server User' } })
+    expect(versions).toEqual(['7.1', '7.1-preview'])
+  })
+
+  it('remembers the -preview requirement per origin after the first rejection', async () => {
+    const versions: (string | null)[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      const url = new URL(String(input))
+      versions.push(url.searchParams.get('api-version'))
+      if (!url.searchParams.get('api-version')?.endsWith('-preview')) {
+        return previewRejection()
+      }
+      return Response.json({ ok: true })
+    }) as never
+
+    const base = 'https://ado-sticky.example.com/tfs/MyCollection'
+    await requestAzureDevOpsJsonAtBase(base, '/_apis/connectionData')
+    await requestAzureDevOpsJsonAtBase(base, '/_apis/connectionData')
+    // First request learns the suffix; the second must not repeat the 400 round trip.
+    expect(versions).toEqual(['7.1', '7.1-preview', '7.1-preview'])
+  })
+
+  it('does not retry a 400 that is not a preview-version rejection', async () => {
+    const fetchMock = vi.fn(async () =>
+      Response.json({ message: 'A project name is required.' }, { status: 400 })
+    )
+    globalThis.fetch = fetchMock as never
+
+    await expect(
+      requestAzureDevOpsJsonAtBase(
+        'https://ado-other.example.com/tfs/Coll',
+        '/_apis/connectionData'
+      )
+    ).resolves.toBeNull()
+    expect(fetchMock).toHaveBeenCalledTimes(1)
+  })
+
+  it('uses the remote-derived project base for Git endpoints when the configured base shares its origin', async () => {
+    process.env.ORCA_AZURE_DEVOPS_API_BASE_URL = SERVER_BASE
+    const paths: string[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      paths.push(new URL(String(input)).pathname)
+      return Response.json({ id: 'repo-guid' })
+    }) as never
+
+    await requestAzureDevOpsJson(serverRepoRef(), '/_apis/git/repositories/my-repo')
+    // Collection-level env base must not strip the project segment Git endpoints need.
+    expect(paths).toEqual(['/tfs/MyCollection/MyProject/_apis/git/repositories/my-repo'])
+  })
+
+  it('keeps a cross-origin configured base URL as an override for Git endpoints', async () => {
+    process.env.ORCA_AZURE_DEVOPS_API_BASE_URL = 'http://127.0.0.1:8123/acme/Project'
+    const origins: string[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      origins.push(new URL(String(input)).origin)
+      return Response.json({ id: 'repo-guid' })
+    }) as never
+
+    await requestAzureDevOpsJson(serverRepoRef(), '/_apis/git/repositories/my-repo')
+    expect(origins).toEqual(['http://127.0.0.1:8123'])
+  })
+
+  it('keeps a same-origin non-ancestor base URL as a Git endpoint override', async () => {
+    process.env.ORCA_AZURE_DEVOPS_API_BASE_URL = 'https://ado.example.com:8443/rewrite/MyProject'
+    const paths: string[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      paths.push(new URL(String(input)).pathname)
+      return Response.json({ id: 'repo-guid' })
+    }) as never
+
+    await requestAzureDevOpsJson(serverRepoRef(), '/_apis/git/repositories/my-repo')
+    expect(paths).toEqual(['/rewrite/MyProject/_apis/git/repositories/my-repo'])
+  })
+})
diff --git a/src/main/azure-devops/azure-devops-api-request.ts b/src/main/azure-devops/azure-devops-api-request.ts
index 5fc8f256793..03c7faac3f4 100644
--- a/src/main/azure-devops/azure-devops-api-request.ts
+++ b/src/main/azure-devops/azure-devops-api-request.ts
@@ -3,6 +3,42 @@ import type { AzureDevOpsRepoRef } from './repository-ref'
 import { cancelUnreadResponseBody } from '../lib/unread-response-body'
 
 const REQUEST_TIMEOUT_MS = 5000
+const DEFAULT_API_VERSION = '7.1'
+
+// Why (STA-3494): on-prem Azure DevOps Server rejects versioned requests without
+// the -preview suffix; remember which origins need it after the first rejection.
+const previewApiVersionOrigins = new Set<string>()
+
+/** @internal - exposed for tests only */
+export function _resetAzureDevOpsPreviewApiVersionCache(): void {
+  previewApiVersionOrigins.clear()
+}
+
+export function markAzureDevOpsPreviewApiVersionOrigin(origin: string): void {
+  previewApiVersionOrigins.add(origin)
+}
+
+export function azureDevOpsApiVersionForOrigin(
+  origin: string,
+  requested?: string | number
+): string {
+  const version = String(requested ?? DEFAULT_API_VERSION)
+  return previewApiVersionOrigins.has(origin) && !version.endsWith('-preview')
+    ? `${version}-preview`
+    : version
+}
+
+export function isAzureDevOpsPreviewVersionRejection(status: number | null, body: string): boolean {
+  if (status !== 400) {
+    return false
+  }
+  try {
+    const parsed = JSON.parse(body) as { typeKey?: unknown } | null
+    return parsed?.typeKey === 'VssInvalidPreviewVersionException'
+  } catch {
+    return false
+  }
+}
 
 type AzureDevOpsAuthConfig = {
   apiBaseUrl: string | null
@@ -52,9 +88,30 @@ function authHeaders(config: AzureDevOpsAuthConfig): Record<string, string> {
   return {}
 }
 
-function configuredApiBaseUrl(repo: AzureDevOpsRepoRef): string {
+function isUrlPathAncestor(ancestor: string, descendant: string): boolean {
+  try {
+    const ancestorUrl = new URL(ancestor)
+    const descendantUrl = new URL(descendant)
+    const ancestorPath = ancestorUrl.pathname.replace(/\/+$/, '')
+    const descendantPath = descendantUrl.pathname.replace(/\/+$/, '')
+    return (
+      ancestorUrl.origin === descendantUrl.origin &&
+      (ancestorPath === descendantPath || descendantPath.startsWith(`${ancestorPath}/`))
+    )
+  } catch {
+    return false
+  }
+}
+
+export function resolveAzureDevOpsGitApiBaseUrl(repo: AzureDevOpsRepoRef): string {
   const configured = getAzureDevOpsAuthConfig().apiBaseUrl
-  return configured ? normalizeAzureDevOpsApiBaseUrl(configured) : repo.apiBaseUrl
+  if (!configured) {
+    return repo.apiBaseUrl
+  }
+  const normalized = normalizeAzureDevOpsApiBaseUrl(configured)
+  // Why (STA-3494): a configured collection ancestor is the auth-probe URL;
+  // Git endpoints need the project-level base derived from the remote.
+  return isUrlPathAncestor(normalized, repo.apiBaseUrl) ? repo.apiBaseUrl : normalized
 }
 
 function apiUrl(
@@ -63,13 +120,32 @@ function apiUrl(
   searchParams?: AzureDevOpsRequestOptions['searchParams']
 ): URL {
   const url = new URL(`${baseUrl.replace(/\/+$/, '')}${path}`)
-  const params = { ...searchParams, 'api-version': searchParams?.['api-version'] ?? '7.1' }
+  const params = {
+    ...searchParams,
+    'api-version': azureDevOpsApiVersionForOrigin(url.origin, searchParams?.['api-version'])
+  }
   for (const [key, value] of Object.entries(params)) {
     url.searchParams.set(key, String(value))
   }
   return url
 }
 
+// Reads the body only for a 400 on a non-preview request; consumed either way.
+async function shouldRetryWithPreviewApiVersion(url: URL, response: Response): Promise<boolean> {
+  if (response.ok || response.status !== 400) {
+    return false
+  }
+  if (url.searchParams.get('api-version')?.endsWith('-preview')) {
+    return false
+  }
+  try {
+    const body = (await response.json()) as { typeKey?: string | null } | null
+    return body?.typeKey === 'VssInvalidPreviewVersionException'
+  } catch {
+    return false
+  }
+}
+
 export async function requestAzureDevOpsJsonAtBase<T>(
   baseUrl: string,
   path: string,
@@ -80,14 +156,21 @@ export async function requestAzureDevOpsJsonAtBase<T>(
   throwOnFailure = false
 ): Promise<T | null> {
   const config = getAzureDevOpsAuthConfig()
-  try {
-    const response = await fetch(apiUrl(baseUrl, path, options.searchParams), {
+  const doFetch = (url: URL): Promise<Response> =>
+    fetch(url, {
       headers: {
         Accept: 'application/json',
         ...authHeaders(config)
       },
       signal: AbortSignal.timeout(options.timeoutMs ?? REQUEST_TIMEOUT_MS)
     })
+  try {
+    const url = apiUrl(baseUrl, path, options.searchParams)
+    let response = await doFetch(url)
+    if (await shouldRetryWithPreviewApiVersion(url, response)) {
+      markAzureDevOpsPreviewApiVersionOrigin(url.origin)
+      response = await doFetch(apiUrl(baseUrl, path, options.searchParams))
+    }
     if (!response.ok) {
       await cancelUnreadResponseBody(response)
       if (throwOnFailure) {
@@ -110,5 +193,10 @@ export function requestAzureDevOpsJson<T>(
   options: AzureDevOpsRequestOptions = {},
   throwOnFailure = false
 ): Promise<T | null> {
-  return requestAzureDevOpsJsonAtBase(configuredApiBaseUrl(repo), path, options, throwOnFailure)
+  return requestAzureDevOpsJsonAtBase(
+    resolveAzureDevOpsGitApiBaseUrl(repo),
+    path,
+    options,
+    throwOnFailure
+  )
 }
diff --git a/src/main/azure-devops/client.test.ts b/src/main/azure-devops/client.test.ts
index b1f857d1bb1..81761bba12f 100644
--- a/src/main/azure-devops/client.test.ts
+++ b/src/main/azure-devops/client.test.ts
@@ -6,6 +6,7 @@ import {
   getAzureDevOpsPullRequestForBranchOrThrow,
   normalizeAzureDevOpsApiBaseUrl
 } from './client'
+import { _resetAzureDevOpsPreviewApiVersionCache } from './azure-devops-api-request'
 import { _resetAzureDevOpsRepoRefCache } from './repository-ref'
 import { __resetRepoDefaultBranchCacheForTests } from '../source-control/repo-default-branch'
 
@@ -39,6 +40,7 @@ describe('Azure DevOps client', () => {
     process.env = { ...OLD_ENV, ORCA_AZURE_DEVOPS_TOKEN: 'pat-token' }
     gitExecFileAsyncMock.mockReset()
     _resetAzureDevOpsRepoRefCache()
+    _resetAzureDevOpsPreviewApiVersionCache()
     __resetRepoDefaultBranchCacheForTests()
   })
 
@@ -65,6 +67,35 @@ describe('Azure DevOps client', () => {
     })
   })
 
+  it('authenticates against an on-prem Server that requires -preview api-versions (STA-3494)', async () => {
+    process.env.ORCA_AZURE_DEVOPS_API_BASE_URL = 'https://ado.example.com:8443/tfs/MyCollection'
+    const versions: (string | null)[] = []
+    globalThis.fetch = vi.fn(async (input: string | URL | Request) => {
+      const url = new URL(String(input))
+      expect(url.pathname).toBe('/tfs/MyCollection/_apis/connectionData')
+      versions.push(url.searchParams.get('api-version'))
+      if (!url.searchParams.get('api-version')?.endsWith('-preview')) {
+        return new Response(
+          JSON.stringify({
+            message: 'The requested version "7.1" of the resource is under preview.',
+            typeKey: 'VssInvalidPreviewVersionException'
+          }),
+          { status: 400, headers: { 'Content-Type': 'application/json' } }
+        )
+      }
+      return Response.json({ authenticatedUser: { providerDisplayName: 'Server User' } })
+    }) as never
+
+    await expect(getAzureDevOpsAuthStatus()).resolves.toEqual({
+      configured: true,
+      authenticated: true,
+      account: 'Server User',
+      baseUrl: 'https://ado.example.com:8443/tfs/MyCollection',
+      tokenConfigured: true
+    })
+    expect(versions).toEqual(['7.1', '7.1-preview'])
+  })
+
   it('resolves a PR for a branch through repository, PR, and status REST calls', async () => {
     gitExecFileAsyncMock.mockResolvedValue({
       stdout: 'https://dev.azure.com/acme/Project/_git/repo\n'
diff --git a/src/main/azure-devops/pull-request-creation.test.ts b/src/main/azure-devops/pull-request-creation.test.ts
index 02a4b4fb74a..7cd401747ff 100644
--- a/src/main/azure-devops/pull-request-creation.test.ts
+++ b/src/main/azure-devops/pull-request-creation.test.ts
@@ -3,6 +3,7 @@ import {
   createAzureDevOpsPullRequest,
   isAzureDevOpsReviewCreationAuthenticated
 } from './pull-request-creation'
+import { _resetAzureDevOpsPreviewApiVersionCache } from './azure-devops-api-request'
 import { _resetAzureDevOpsRepoRefCache } from './repository-ref'
 import { REMOTE_URL_PROBE_TIMEOUT_MS } from '../git/remote-url-probe'
 
@@ -37,6 +38,7 @@ describe('Azure DevOps pull request creation', () => {
       stderr: ''
     })
     _resetAzureDevOpsRepoRefCache()
+    _resetAzureDevOpsPreviewApiVersionCache()
   })
 
   afterEach(() => {
@@ -98,6 +100,77 @@ describe('Azure DevOps pull request creation', () => {
     expect(fetchMock).toHaveBeenCalledOnce()
   })
 
+  it('retries PR creation with -preview when the Server rejects the api-version (STA-3494)', async () => {
+    gitExecFileAsyncMock.mockResolvedValue({
+      stdout: 'https://ado.example.com:8443/tfs/MyCollection/MyProject/_git/my-repo\n',
+      stderr: ''
+    })
+    const versions: (string | null)[] = []
+    const fetchMock = vi.fn(async (input: string | URL | Request) => {
+      const url = new URL(String(input))
+      expect(url.pathname).toBe(
+        '/tfs/MyCollection/MyProject/_apis/git/repositories/my-repo/pullRequests'
+      )
+      versions.push(url.searchParams.get('api-version'))
+      if (!url.searchParams.get('api-version')?.endsWith('-preview')) {
+        return new Response(
+          JSON.stringify({
+            message: 'The requested version "7.1" of the resource is under preview.',
+            typeKey: 'VssInvalidPreviewVersionException'
+          }),
+          { status: 400, headers: { 'Content-Type': 'application/json' } }
+        )
+      }
+      return Response.json({
+        pullRequestId: 51,
+        title: 'Server create',
+        status: 'active',
+        creationDate: '2026-06-01T00:00:00Z',
+        _links: {
+          web: {
+            href: 'https://ado.example.com:8443/tfs/MyCollection/MyProject/_git/my-repo/pullrequest/51'
+          }
+        }
+      })
+    })
+    globalThis.fetch = fetchMock as never
+
+    await expect(
+      createAzureDevOpsPullRequest('/repo', {
+        provider: 'azure-devops',
+        base: 'main',
+        head: 'feature/server',
+        title: 'Server create',
+        body: 'Body'
+      })
+    ).resolves.toEqual({
+      ok: true,
+      number: 51,
+      url: 'https://ado.example.com:8443/tfs/MyCollection/MyProject/_git/my-repo/pullrequest/51'
+    })
+    expect(versions).toEqual(['7.1', '7.1-preview'])
+  })
+
+  it('does not retry PR creation when only the error message names the preview exception', async () => {
+    const fetchMock = vi.fn(async () =>
+      Response.json(
+        { message: 'Validation failed near VssInvalidPreviewVersionException' },
+        { status: 400 }
+      )
+    )
+    globalThis.fetch = fetchMock as never
+
+    await expect(
+      createAzureDevOpsPullRequest('/repo', {
+        provider: 'azure-devops',
+        base: 'main',
+        head: 'feature/azure',
+        title: 'Do not retry'
+      })
+    ).resolves.toMatchObject({ ok: false, code: 'validation' })
+    expect(fetchMock).toHaveBeenCalledOnce()
+  })
+
   it('resolves Azure DevOps remotes through the SSH git provider', async () => {
     const remoteGit = {
       exec: vi.fn(async () => ({
diff --git a/src/main/azure-devops/pull-request-creation.ts b/src/main/azure-devops/pull-request-creation.ts
index 7a3f25c13a3..e190e65a462 100644
--- a/src/main/azure-devops/pull-request-creation.ts
+++ b/src/main/azure-devops/pull-request-creation.ts
@@ -9,6 +9,12 @@ import {
   requestHostedReviewJson
 } from '../source-control/hosted-review-api-request'
 import { readHostedPullRequestTemplate } from '../source-control/pull-request-template'
+import {
+  azureDevOpsApiVersionForOrigin,
+  isAzureDevOpsPreviewVersionRejection,
+  markAzureDevOpsPreviewApiVersionOrigin,
+  resolveAzureDevOpsGitApiBaseUrl
+} from './azure-devops-api-request'
 import { getAzureDevOpsPullRequestForBranch } from './client'
 import { mapAzureDevOpsPullRequest, type RawAzureDevOpsPullRequest } from './pull-request-mappers'
 import { getAzureDevOpsRepoRef, type AzureDevOpsRepoRef } from './repository-ref'
@@ -16,7 +22,6 @@ import { getAzureDevOpsRepoRef, type AzureDevOpsRepoRef } from './repository-ref
 const CREATE_REQUEST_TIMEOUT_MS = 60_000
 
 type AzureDevOpsCreateAuthConfig = {
-  apiBaseUrl: string | null
   pat: string | null
   accessToken: string | null
   username: string | null
@@ -27,16 +32,8 @@ function envValue(name: string): string | null {
   return value.length > 0 ? value : null
 }
 
-function normalizeApiBaseUrl(value: string): string {
-  return value
-    .trim()
-    .replace(/\/+$/, '')
-    .replace(/\/_apis$/i, '')
-}
-
 function getAuthConfig(): AzureDevOpsCreateAuthConfig {
   return {
-    apiBaseUrl: envValue('ORCA_AZURE_DEVOPS_API_BASE_URL'),
     pat: envValue('ORCA_AZURE_DEVOPS_TOKEN') ?? envValue('ORCA_AZURE_DEVOPS_PAT'),
     accessToken: envValue('ORCA_AZURE_DEVOPS_ACCESS_TOKEN'),
     username: envValue('ORCA_AZURE_DEVOPS_USERNAME')
@@ -60,13 +57,43 @@ function authHeaders(config: AzureDevOpsCreateAuthConfig): Record<string, string
 }
 
 function apiUrl(repo: AzureDevOpsRepoRef, path: string): URL {
-  const config = getAuthConfig()
-  const baseUrl = config.apiBaseUrl ? normalizeApiBaseUrl(config.apiBaseUrl) : repo.apiBaseUrl
+  const baseUrl = resolveAzureDevOpsGitApiBaseUrl(repo)
   const url = new URL(`${baseUrl.replace(/\/+$/, '')}${path}`)
-  url.searchParams.set('api-version', '7.1')
+  url.searchParams.set('api-version', azureDevOpsApiVersionForOrigin(url.origin))
   return url
 }
 
+// Why (STA-3494): Azure DevOps Server 400s versioned requests without -preview;
+// the rejection happens before the PR is created, so one retry is safe.
+async function requestCreatePullRequest(
+  repo: AzureDevOpsRepoRef,
+  path: string,
+  init: Omit<RequestInit, 'signal'>
+): Promise<RawAzureDevOpsPullRequest> {
+  const url = apiUrl(repo, path)
+  try {
+    return await requestHostedReviewJson<RawAzureDevOpsPullRequest>(
+      url,
+      init,
+      CREATE_REQUEST_TIMEOUT_MS
+    )
+  } catch (error) {
+    if (
+      url.searchParams.get('api-version')?.endsWith('-preview') ||
+      !(error instanceof HostedReviewApiRequestError) ||
+      !isAzureDevOpsPreviewVersionRejection(error.status, error.message)
+    ) {
+      throw error
+    }
+    markAzureDevOpsPreviewApiVersionOrigin(url.origin)
+    return requestHostedReviewJson<RawAzureDevOpsPullRequest>(
+      apiUrl(repo, path),
+      init,
+      CREATE_REQUEST_TIMEOUT_MS
+    )
+  }
+}
+
 function encodePathSegment(value: string): string {
   return encodeURIComponent(value)
 }
@@ -192,8 +219,9 @@ export async function createAzureDevOpsPullRequest(
   }
 
   try {
-    const raw = await requestHostedReviewJson<RawAzureDevOpsPullRequest>(
-      apiUrl(repo, `/_apis/git/repositories/${encodePathSegment(repo.repository)}/pullRequests`),
+    const raw = await requestCreatePullRequest(
+      repo,
+      `/_apis/git/repositories/${encodePathSegment(repo.repository)}/pullRequests`,
       {
         method: 'POST',
         headers: {
@@ -202,8 +230,7 @@ export async function createAzureDevOpsPullRequest(
           ...authHeaders(getAuthConfig())
         },
         body: JSON.stringify(requestBody)
-      },
-      CREATE_REQUEST_TIMEOUT_MS
+      }
     )
     const created = mapAzureDevOpsPullRequest(raw, 'neutral', repo.webBaseUrl)
     if (created) {