diff --git a/src/main/runtime/orca-runtime-files-watch.test.ts b/src/main/runtime/orca-runtime-files-watch.test.ts
index 80fb652227d..7611178f6ca 100644
--- a/src/main/runtime/orca-runtime-files-watch.test.ts
+++ b/src/main/runtime/orca-runtime-files-watch.test.ts
@@ -52,6 +52,13 @@ function createRuntimeFileCommands(rootPath: string) {
       repoId: 'repo-1',
       path: rootPath
     })),
+    resolveRuntimeFileTarget: vi.fn(async () => ({
+      worktree: {
+        id: 'wt-1',
+        repoId: 'repo-1',
+        path: rootPath
+      }
+    })),
     resolveRuntimeGitTarget: vi.fn(),
     openFile: vi.fn()
   } as never)
diff --git a/src/main/runtime/orca-runtime-files.test.ts b/src/main/runtime/orca-runtime-files.test.ts
index c794fbf3998..dbc4a94dce0 100644
--- a/src/main/runtime/orca-runtime-files.test.ts
+++ b/src/main/runtime/orca-runtime-files.test.ts
@@ -126,20 +126,28 @@ function createRuntimeFileCommands(options?: {
   path?: string
   openFile?: ReturnType<typeof vi.fn>
   openDiff?: ReturnType<typeof vi.fn>
+  resolveRuntimeFileTarget?: ReturnType<typeof vi.fn>
   resolveRuntimeGitTarget?: ReturnType<typeof vi.fn>
 }) {
   const store = {
     getRepo: vi.fn((_repoId?: string) => undefined as { connectionId?: string } | undefined)
   }
   const path = options?.path ?? '/repo'
+  const worktree = {
+    id: 'wt-1',
+    repoId: 'repo-1',
+    path
+  }
   const commands = new RuntimeFileCommands({
     getRuntimeId: () => 'runtime-1',
     requireStore: () => store,
-    resolveWorktreeSelector: vi.fn(async () => ({
-      id: 'wt-1',
-      repoId: 'repo-1',
-      path
-    })),
+    resolveWorktreeSelector: vi.fn(async () => worktree),
+    resolveRuntimeFileTarget:
+      options?.resolveRuntimeFileTarget ??
+      vi.fn(async () => ({
+        worktree,
+        connectionId: store.getRepo(worktree.repoId)?.connectionId
+      })),
     resolveRuntimeGitTarget: options?.resolveRuntimeGitTarget ?? vi.fn(),
     openFile: options?.openFile ?? vi.fn(),
     ...(options?.openDiff ? { openDiff: options.openDiff } : {})
@@ -427,7 +435,7 @@ describe('RuntimeFileCommands', () => {
   })
 
   it('settles and detaches runtime rg searches when timeout kill is ignored', async () => {
-    const resolveRuntimeGitTarget = vi.fn(async () => ({
+    const resolveRuntimeFileTarget = vi.fn(async () => ({
       worktree: {
         id: 'wt-1',
         repoId: 'repo-1',
@@ -435,7 +443,7 @@ describe('RuntimeFileCommands', () => {
       },
       connectionId: null
     }))
-    const { commands } = createRuntimeFileCommands({ resolveRuntimeGitTarget })
+    const { commands } = createRuntimeFileCommands({ resolveRuntimeFileTarget })
     const child = createRuntimeSearchChild()
     resolveAuthorizedPathMock.mockResolvedValue('/repo')
     checkRgAvailableMock.mockResolvedValue(true)
@@ -460,7 +468,7 @@ describe('RuntimeFileCommands', () => {
   })
 
   it('routes runtime rg searches through the registered WSL project runtime', async () => {
-    const resolveRuntimeGitTarget = vi.fn(async () => ({
+    const resolveRuntimeFileTarget = vi.fn(async () => ({
       worktree: {
         id: 'wt-1',
         repoId: 'repo-1',
@@ -468,7 +476,7 @@ describe('RuntimeFileCommands', () => {
       },
       connectionId: null
     }))
-    const { commands, store } = createRuntimeFileCommands({ resolveRuntimeGitTarget })
+    const { commands, store } = createRuntimeFileCommands({ resolveRuntimeFileTarget })
     const child = createRuntimeSearchChild()
     resolveAuthorizedPathMock.mockResolvedValue('C:\\repo')
     checkRgAvailableMock.mockResolvedValue(true)
diff --git a/src/main/runtime/orca-runtime-files.ts b/src/main/runtime/orca-runtime-files.ts
index 5b4c6047c2d..07135039e63 100644
--- a/src/main/runtime/orca-runtime-files.ts
+++ b/src/main/runtime/orca-runtime-files.ts
@@ -143,11 +143,16 @@ export async function awaitRuntimeFileWatcherUnsubscribes(): Promise<void> {
 }
 
 export type ResolvedRuntimeFileWorktree = Worktree & { git: GitWorktreeInfo }
+export type ResolvedRuntimeFileTarget = {
+  worktree: ResolvedRuntimeFileWorktree
+  connectionId?: string
+}
 
 export type RuntimeFileCommandHost = {
   getRuntimeId(): string
   requireStore(): Store
   resolveWorktreeSelector(selector: string): Promise<ResolvedRuntimeFileWorktree>
+  resolveRuntimeFileTarget(selector: string): Promise<ResolvedRuntimeFileTarget>
   resolveRuntimeGitTarget(
     selector: string
   ): Promise<{ worktree: ResolvedRuntimeFileWorktree; connectionId?: string }>
@@ -173,9 +178,8 @@ export class RuntimeFileCommands {
 
   async listMobileFiles(worktreeSelector: string): Promise<RuntimeFileListResult> {
     const store = this.host.requireStore()
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
-    const repo = store.getRepo(worktree.repoId)
-    const connectionId = repo?.connectionId ?? undefined
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
+    const { worktree, connectionId } = target
     const files = connectionId
       ? await this.listRemoteMobileFiles(worktree.path, connectionId)
       : await listQuickOpenFiles(worktree.path, store)
@@ -202,7 +206,7 @@ export class RuntimeFileCommands {
     worktreeSelector: string,
     relativePath: string
   ): Promise<RuntimeFileOpenResult> {
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
+    const { worktree } = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     if (!isSafeMobileRelativePath(relativePath)) {
       throw new Error('invalid_relative_path')
     }
@@ -234,7 +238,7 @@ export class RuntimeFileCommands {
     relativePath: string,
     staged: boolean
   ): Promise<RuntimeFileOpenResult> {
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
+    const { worktree } = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     if (!isSafeMobileRelativePath(relativePath)) {
       throw new Error('invalid_relative_path')
     }
@@ -254,7 +258,8 @@ export class RuntimeFileCommands {
     relativePath: string
   ): Promise<RuntimeFileReadResult> {
     const store = this.host.requireStore()
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
+    const { worktree, connectionId } = target
     if (!isSafeMobileRelativePath(relativePath)) {
       throw new Error('invalid_relative_path')
     }
@@ -262,10 +267,9 @@ export class RuntimeFileCommands {
       throw new Error('binary_file')
     }
 
-    const repo = store.getRepo(worktree.repoId)
     const filePath = joinWorktreeRelativePath(worktree.path, relativePath)
-    const content = repo?.connectionId
-      ? await this.readRemoteMobileFile(filePath, repo.connectionId)
+    const content = connectionId
+      ? await this.readRemoteMobileFile(filePath, connectionId)
       : await readLocalMobileFile(filePath, store)
     const truncated = truncateMobileFilePreview(content)
 
@@ -291,9 +295,8 @@ export class RuntimeFileCommands {
     cwd?: string | null
   ): Promise<RuntimeTerminalPathResolution> {
     const store = this.host.requireStore()
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
-    const repo = store.getRepo(worktree.repoId)
-    const connectionId = repo?.connectionId ?? undefined
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
+    const { worktree, connectionId } = target
     const base = cwd && cwd.trim().length > 0 ? cwd : worktree.path
 
     const empty: RuntimeTerminalPathResolution = {
@@ -764,7 +767,7 @@ export class RuntimeFileCommands {
     worktreeSelector: string,
     options: Omit<SearchOptions, 'rootPath'>
   ): Promise<SearchResult> {
-    const target = await this.host.resolveRuntimeGitTarget(worktreeSelector)
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     const provider = target.connectionId ? getSshFilesystemProvider(target.connectionId) : null
     const rootPath = target.worktree.path
     const searchOptions = { ...options, rootPath }
@@ -781,7 +784,7 @@ export class RuntimeFileCommands {
     worktreeSelector: string,
     options: { excludePaths?: string[] } = {}
   ): Promise<string[]> {
-    const target = await this.host.resolveRuntimeGitTarget(worktreeSelector)
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     const provider = target.connectionId ? getSshFilesystemProvider(target.connectionId) : null
     if (target.connectionId) {
       if (!provider) {
@@ -793,7 +796,7 @@ export class RuntimeFileCommands {
   }
 
   async listRuntimeMarkdownDocuments(worktreeSelector: string): Promise<MarkdownDocument[]> {
-    const target = await this.host.resolveRuntimeGitTarget(worktreeSelector)
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     const provider = target.connectionId ? getSshFilesystemProvider(target.connectionId) : null
     if (target.connectionId) {
       if (!provider) {
@@ -943,14 +946,12 @@ export class RuntimeFileCommands {
     worktreeSelector: string,
     relativePath: string
   ): Promise<{ worktree: ResolvedRuntimeFileWorktree; path: string; connectionId?: string }> {
-    const store = this.host.requireStore()
-    const worktree = await this.host.resolveWorktreeSelector(worktreeSelector)
+    const target = await this.host.resolveRuntimeFileTarget(worktreeSelector)
     const normalizedRelativePath = normalizeRuntimeRelativePath(relativePath)
-    const repo = store.getRepo(worktree.repoId)
     return {
-      worktree,
-      path: joinWorktreeRelativePath(worktree.path, normalizedRelativePath),
-      connectionId: repo?.connectionId ?? undefined
+      worktree: target.worktree,
+      path: joinWorktreeRelativePath(target.worktree.path, normalizedRelativePath),
+      connectionId: target.connectionId
     }
   }
 
diff --git a/src/main/runtime/orca-runtime.test.ts b/src/main/runtime/orca-runtime.test.ts
index 3aa0b1f5688..c1e9fdecb5e 100644
--- a/src/main/runtime/orca-runtime.test.ts
+++ b/src/main/runtime/orca-runtime.test.ts
@@ -360,7 +360,8 @@ vi.mock('../ipc/worktree-logic', async (importOriginal) => {
 vi.mock('../ipc/filesystem-auth', () => ({
   invalidateAuthorizedRootsCache: invalidateAuthorizedRootsCacheMock,
   isENOENT: (error: unknown) =>
-    Boolean(error && typeof error === 'object' && 'code' in error && error.code === 'ENOENT')
+    Boolean(error && typeof error === 'object' && 'code' in error && error.code === 'ENOENT'),
+  resolveAuthorizedPath: vi.fn(async (pathValue: string) => pathValue)
 }))
 
 vi.mock('../worktree-root-preparation', () => ({
@@ -1867,6 +1868,74 @@ describe('OrcaRuntimeService', () => {
     expect(gitProvider.getStatus).toHaveBeenCalledWith('//Server/Share/Repo')
   })
 
+  it.each([
+    { label: 'canonical folder workspace selector', selector: TEST_FOLDER_WORKSPACE_KEY },
+    { label: 'id-prefixed folder workspace selector', selector: `id:${TEST_FOLDER_WORKSPACE_KEY}` }
+  ])('reads file explorer paths for a $label', async ({ selector }) => {
+    const folderPath = await mkdtemp(join(tmpdir(), 'orca-runtime-folder-files-'))
+    await mkdir(join(folderPath, 'src'))
+    await writeFile(join(folderPath, 'src', 'app.ts'), 'export {}\n')
+    const folderWorkspace = makeFolderWorkspace({ folderPath })
+    const projectGroup = makeFolderProjectGroup({ parentPath: folderPath })
+    const runtime = new OrcaRuntimeService(
+      createFolderWorkspaceRuntimeStore(folderWorkspace, projectGroup) as never
+    )
+
+    await expect(runtime.readFileExplorerDir(selector, 'src')).resolves.toContainEqual({
+      name: 'app.ts',
+      isDirectory: false,
+      isSymlink: false
+    })
+    await expect(runtime.readFileExplorerPreview(selector, 'src/app.ts')).resolves.toMatchObject({
+      content: 'export {}\n',
+      isBinary: false
+    })
+  })
+
+  it('routes SSH folder workspace file explorer paths through the filesystem provider', async () => {
+    const folderPath = '/srv/platform'
+    const fsProvider = {
+      stat: vi.fn(async (pathValue: string) => ({
+        size: pathValue.endsWith('/app.ts') ? 8 : 0,
+        type: pathValue.endsWith('/app.ts') ? 'file' : 'directory',
+        mtime: 1
+      })),
+      readDir: vi.fn().mockResolvedValue([
+        {
+          name: 'app.ts',
+          isDirectory: false,
+          isSymlink: false
+        }
+      ]),
+      readFile: vi.fn().mockResolvedValue({ content: 'remote\n', isBinary: false })
+    }
+    const folderWorkspace = makeFolderWorkspace({ folderPath, connectionId: 'ssh-folder' })
+    const projectGroup = makeFolderProjectGroup({ parentPath: folderPath })
+    const runtime = new OrcaRuntimeService(
+      createFolderWorkspaceRuntimeStore(folderWorkspace, projectGroup) as never
+    )
+    registerSshFilesystemProvider('ssh-folder', fsProvider as never)
+
+    try {
+      await expect(
+        runtime.readFileExplorerDir(`id:${TEST_FOLDER_WORKSPACE_KEY}`, 'src')
+      ).resolves.toHaveLength(1)
+      await expect(
+        runtime.readFileExplorerPreview(`id:${TEST_FOLDER_WORKSPACE_KEY}`, 'src/app.ts')
+      ).resolves.toMatchObject({
+        content: 'remote\n',
+        isBinary: false
+      })
+    } finally {
+      unregisterSshFilesystemProvider('ssh-folder')
+    }
+
+    expect(fsProvider.stat).toHaveBeenCalledWith(folderPath)
+    expect(fsProvider.readDir).toHaveBeenCalledWith('/srv/platform/src')
+    expect(fsProvider.stat).toHaveBeenCalledWith('/srv/platform/src/app.ts')
+    expect(fsProvider.readFile).toHaveBeenCalledWith('/srv/platform/src/app.ts')
+  })
+
   it('lists persisted SSH worktrees while the git provider is unavailable', async () => {
     vi.mocked(listWorktrees).mockClear()
     const remoteRepo = {
diff --git a/src/main/runtime/orca-runtime.ts b/src/main/runtime/orca-runtime.ts
index 4c421345834..f724e6ee88b 100644
--- a/src/main/runtime/orca-runtime.ts
+++ b/src/main/runtime/orca-runtime.ts
@@ -4675,6 +4675,7 @@ export class OrcaRuntimeService {
     getRuntimeId: () => this.runtimeId,
     requireStore: () => this.requireStore(),
     resolveWorktreeSelector: (selector) => this.resolveWorktreeSelector(selector),
+    resolveRuntimeFileTarget: (selector) => this.resolveRuntimeFileTarget(selector),
     resolveRuntimeGitTarget: (selector) => this.resolveRuntimeGitTarget(selector),
     openFile: (worktreeId, filePath, relativePath, runtimeEnvironmentId) => {
       if (!this.notifier?.openFile) {
@@ -4836,6 +4837,24 @@ export class OrcaRuntimeService {
     return { worktree, repo, connectionId, localGitOptions }
   }
 
+  private async resolveRuntimeFileTarget(worktreeSelector: string): Promise<{
+    worktree: ResolvedWorktree
+    connectionId?: string
+  }> {
+    const folderScope = await this.resolveFolderWorkspaceLaunchScope(worktreeSelector)
+    if (folderScope?.folderWorkspace) {
+      return {
+        worktree: this.folderWorkspaceToResolvedWorktree(folderScope.folderWorkspace),
+        connectionId: folderScope.connectionId ?? undefined
+      }
+    }
+
+    const store = this.requireStore()
+    const worktree = await this.resolveWorktreeSelector(worktreeSelector)
+    const repo = store.getRepo(worktree.repoId)
+    return { worktree, connectionId: repo?.connectionId ?? undefined }
+  }
+
   onMobileSessionTabsChanged(
     listener: (snapshot: RuntimeMobileSessionTabsResult) => void
   ): () => void {
@@ -16024,6 +16043,23 @@ export class OrcaRuntimeService {
     }
   }
 
+  private folderWorkspaceToResolvedWorktree(folderWorkspace: FolderWorkspace): ResolvedWorktree {
+    const worktree = folderWorkspaceToWorktree(folderWorkspace)
+    return {
+      ...worktree,
+      parentWorktreeId: null,
+      childWorktreeIds: [],
+      lineage: null,
+      git: {
+        path: worktree.path,
+        head: worktree.head,
+        branch: worktree.branch,
+        isBare: worktree.isBare,
+        isMainWorktree: worktree.isMainWorktree
+      }
+    }
+  }
+
   private async resolveTerminalWorkspaceLaunchScope(
     selector: string
   ): Promise<TerminalWorkspaceLaunchScope> {