diff --git a/src/main/runtime/orca-runtime-files.test.ts b/src/main/runtime/orca-runtime-files.test.ts
index 313b3a7bd..6d8809cf4 100644
--- a/src/main/runtime/orca-runtime-files.test.ts
+++ b/src/main/runtime/orca-runtime-files.test.ts
@@ -182,7 +182,7 @@ describe('RuntimeFileCommands', () => {
     vi.useRealTimers()
   })
 
-  it('opens source control diffs through the renderer host', async () => {
+  it('opens source control diffs through the renderer host (inheriting active runtime env)', async () => {
     const openDiff = vi.fn()
     const { commands } = createRuntimeFileCommands({ openDiff })
 
@@ -193,7 +193,7 @@ describe('RuntimeFileCommands', () => {
       '/repo/docs/readme.md',
       'docs/readme.md',
       true,
-      'runtime-1'
+      undefined
     )
     expect(result).toEqual({
       worktree: 'wt-1',
@@ -203,7 +203,7 @@ describe('RuntimeFileCommands', () => {
     })
   })
 
-  it('opens text files through the renderer host with the runtime owner', async () => {
+  it('opens text files through the renderer host (inheriting active runtime env)', async () => {
     const openFile = vi.fn()
     const { commands } = createRuntimeFileCommands({ openFile })
 
@@ -213,7 +213,7 @@ describe('RuntimeFileCommands', () => {
       'wt-1',
       '/repo/docs/readme.md',
       'docs/readme.md',
-      'runtime-1'
+      undefined
     )
     expect(result).toEqual({
       worktree: 'wt-1',
diff --git a/src/main/runtime/orca-runtime-files.ts b/src/main/runtime/orca-runtime-files.ts
index dc5738a4e..99aab104b 100644
--- a/src/main/runtime/orca-runtime-files.ts
+++ b/src/main/runtime/orca-runtime-files.ts
@@ -124,14 +124,14 @@ export type RuntimeFileCommandHost = {
     worktreeId: string,
     filePath: string,
     relativePath: string,
-    runtimeEnvironmentId: string
+    runtimeEnvironmentId?: string | null
   ): void
   openDiff(
     worktreeId: string,
     filePath: string,
     relativePath: string,
     staged: boolean,
-    runtimeEnvironmentId: string
+    runtimeEnvironmentId?: string | null
   ): void
 }
 
@@ -184,7 +184,13 @@ export class RuntimeFileCommands {
       return { worktree: worktree.id, relativePath, kind, opened: false }
     }
     const filePath = joinWorktreeRelativePath(worktree.path, relativePath)
-    this.host.openFile(worktree.id, filePath, relativePath, this.host.getRuntimeId())
+    // Why: the service's internal runtimeId is not a registered runtime env selector
+    // (those live in orca-environments.json). Passing it caused Unknown environment
+    // errors on content load for CLI-initiated opens (via files.open from orca cli
+    // used by agents). Instead pass undefined so the renderer openFile falls back to
+    // the current activeRuntimeEnvironmentId (or null), matching sidebar opens and
+    // allowing correct routing for local vs remote envs.
+    this.host.openFile(worktree.id, filePath, relativePath, undefined)
     return { worktree: worktree.id, relativePath, kind, opened: true }
   }
 
@@ -203,7 +209,8 @@ export class RuntimeFileCommands {
         ? 'markdown'
         : 'text'
     const filePath = joinWorktreeRelativePath(worktree.path, relativePath)
-    this.host.openDiff(worktree.id, filePath, relativePath, staged, this.host.getRuntimeId())
+    // Why: see openMobileFile; avoid stamping internal runtimeId as runtimeEnvironmentId.
+    this.host.openDiff(worktree.id, filePath, relativePath, staged, undefined)
     return { worktree: worktree.id, relativePath, kind, opened: true }
   }
 
diff --git a/src/main/runtime/orca-runtime.ts b/src/main/runtime/orca-runtime.ts
index 29a6ab038..2444fe05a 100644
--- a/src/main/runtime/orca-runtime.ts
+++ b/src/main/runtime/orca-runtime.ts
@@ -790,14 +790,14 @@ type RuntimeNotifier = {
     worktreeId: string,
     filePath: string,
     relativePath: string,
-    runtimeEnvironmentId: string
+    runtimeEnvironmentId?: string | null
   ): void
   openDiff?(
     worktreeId: string,
     filePath: string,
     relativePath: string,
     staged: boolean,
-    runtimeEnvironmentId: string
+    runtimeEnvironmentId?: string | null
   ): void
   readMobileMarkdownTab?(worktreeId: string, tabId: string): Promise<RuntimeMarkdownReadTabResult>
   saveMobileMarkdownTab?(
diff --git a/src/main/window/attach-main-window-services.ts b/src/main/window/attach-main-window-services.ts
index 478cc1638..4b03bcdd1 100644
--- a/src/main/window/attach-main-window-services.ts
+++ b/src/main/window/attach-main-window-services.ts
@@ -272,14 +272,14 @@ function registerRuntimeWindowLifecycle(
     closeSessionTab: (tabId, worktreeId) => send('ui:closeSessionTab', { tabId, worktreeId }),
     moveSessionTab: (worktreeId: string, move: RuntimeMobileSessionTabMove) =>
       send('ui:moveSessionTab', { worktreeId, ...move }),
-    openFile: (worktreeId, filePath, relativePath, runtimeEnvironmentId) =>
+    openFile: (worktreeId, filePath, relativePath, runtimeEnvironmentId?) =>
       send('ui:openFileFromMobile', {
         worktreeId,
         filePath,
         relativePath,
         runtimeEnvironmentId
       }),
-    openDiff: (worktreeId, filePath, relativePath, staged, runtimeEnvironmentId) =>
+    openDiff: (worktreeId, filePath, relativePath, staged, runtimeEnvironmentId?) =>
       send('ui:openDiffFromMobile', {
         worktreeId,
         filePath,
diff --git a/src/preload/api-types.ts b/src/preload/api-types.ts
index 0a735bc10..5d67fda2c 100644
--- a/src/preload/api-types.ts
+++ b/src/preload/api-types.ts
@@ -2167,7 +2167,7 @@ export type PreloadApi = {
         worktreeId: string
         filePath: string
         relativePath: string
-        runtimeEnvironmentId: string
+        runtimeEnvironmentId?: string
       }) => void
     ) => () => void
     onOpenDiffFromMobile: (
@@ -2176,7 +2176,7 @@ export type PreloadApi = {
         filePath: string
         relativePath: string
         staged: boolean
-        runtimeEnvironmentId: string
+        runtimeEnvironmentId?: string
       }) => void
     ) => () => void
     onMobileMarkdownRequest: (
diff --git a/src/preload/index.ts b/src/preload/index.ts
index b968e9e66..a77c9ecbf 100644
--- a/src/preload/index.ts
+++ b/src/preload/index.ts
@@ -2851,7 +2851,7 @@ const api = {
         worktreeId: string
         filePath: string
         relativePath: string
-        runtimeEnvironmentId: string
+        runtimeEnvironmentId?: string
       }) => void
     ): (() => void) => {
       const listener = (
@@ -2860,7 +2860,7 @@ const api = {
           worktreeId: string
           filePath: string
           relativePath: string
-          runtimeEnvironmentId: string
+          runtimeEnvironmentId?: string
         }
       ) => callback(data)
       ipcRenderer.on('ui:openFileFromMobile', listener)
@@ -2872,7 +2872,7 @@ const api = {
         filePath: string
         relativePath: string
         staged: boolean
-        runtimeEnvironmentId: string
+        runtimeEnvironmentId?: string
       }) => void
     ): (() => void) => {
       const listener = (
@@ -2882,7 +2882,7 @@ const api = {
           filePath: string
           relativePath: string
           staged: boolean
-          runtimeEnvironmentId: string
+          runtimeEnvironmentId?: string
         }
       ) => callback(data)
       ipcRenderer.on('ui:openDiffFromMobile', listener)