diff --git a/src/main/runtime/orca-runtime-invalidate-all-handles-for-pty.ts b/src/main/runtime/orca-runtime-invalidate-all-handles-for-pty.ts
index 448fb2a00fb..9d6e5d56ca4 100644
--- a/src/main/runtime/orca-runtime-invalidate-all-handles-for-pty.ts
+++ b/src/main/runtime/orca-runtime-invalidate-all-handles-for-pty.ts
@@ -1,6 +1,12 @@
 // @ts-nocheck -- mechanically split from OrcaRuntimeService; behavior is covered by AST equivalence and characterization tests.
 import { OrcaRuntimeWithResolveKnownWorkspaceFileTarget } from './orca-runtime-resolve-known-workspace-file-target'
 import type { PtyIncarnationId } from '../../shared/pty-incarnation'
+import { getPtyExecutionHost } from '../../shared/terminal-execution-host'
+import {
+  LOCAL_EXECUTION_HOST_ID,
+  parseExecutionHostId,
+  toSshExecutionHostId
+} from '../../shared/execution-host'
 
 export class OrcaRuntimeWithInvalidateAllHandlesForPty extends OrcaRuntimeWithResolveKnownWorkspaceFileTarget {
   protected invalidateAllHandlesForPty(ptyId: string, preserveHandle?: string): Set<string> {
@@ -110,11 +116,30 @@ export class OrcaRuntimeWithInvalidateAllHandlesForPty extends OrcaRuntimeWithRe
     return false
   }
 
+  protected invalidatePtyControllerInventoryForLifecycle(
+    ptyId: string,
+    connectionId?: string | null
+  ): void {
+    const generation = ++this.ptyControllerInventorySequence
+    const hostId = getPtyExecutionHost(ptyId)
+    if (hostId === 'foreign' || (hostId && parseExecutionHostId(hostId)?.kind === 'runtime')) {
+      this.ptyControllerAggregateInventoryGeneration = generation
+      return
+    }
+    const connection =
+      connectionId === undefined ? this.ptysById.get(ptyId)?.connectionId : connectionId
+    const providerKey =
+      hostId ?? (connection ? toSshExecutionHostId(connection) : LOCAL_EXECUTION_HOST_ID)
+    // A pending census predates this admission or exit, including legacy IDs without an incarnation.
+    this.ptyControllerInventoryGenerationByProvider.set(providerKey, generation)
+  }
+
   onPtySpawned(
     ptyId: string,
     incarnationId?: PtyIncarnationId,
     options: { awaitsRegistration?: boolean } = {}
   ): void {
+    this.invalidatePtyControllerInventoryForLifecycle(ptyId)
     const existingPty = this.ptysById.get(ptyId)
     if (
       existingPty &&
diff --git a/src/main/runtime/orca-runtime-on-pty-exit.ts b/src/main/runtime/orca-runtime-on-pty-exit.ts
index 6ddf877f87c..ce24ed65d98 100644
--- a/src/main/runtime/orca-runtime-on-pty-exit.ts
+++ b/src/main/runtime/orca-runtime-on-pty-exit.ts
@@ -30,6 +30,7 @@ export class OrcaRuntimeWithOnPtyExit extends OrcaRuntimeWithOnClientDisconnecte
     if (exitIncarnationId && pty?.incarnationId && exitIncarnationId !== pty.incarnationId) {
       return
     }
+    this.invalidatePtyControllerInventoryForLifecycle(ptyId, pty?.connectionId)
     // A bare exit code is not enough to establish why a process ended: older
     // daemons and SSH relays can report 0 for crashes and wrapper exits.
     const observedCause = options.cause ?? resolveUnreportedExitCause(exitCode)
diff --git a/src/main/runtime/orca-runtime-refresh-pty-worktree-records-with-controller-inventory.ts b/src/main/runtime/orca-runtime-refresh-pty-worktree-records-with-controller-inventory.ts
index aca67f67ba2..930907da120 100644
--- a/src/main/runtime/orca-runtime-refresh-pty-worktree-records-with-controller-inventory.ts
+++ b/src/main/runtime/orca-runtime-refresh-pty-worktree-records-with-controller-inventory.ts
@@ -55,7 +55,10 @@ export class OrcaRuntimeWithRefreshPtyWorktreeRecordsWithControllerInventory ext
     }
     const inventoryGeneration = this.ptyControllerInventorySequence + 1
     this.ptyControllerInventorySequence = inventoryGeneration
-    const providerKey = typeof connectionId === 'string' ? `ssh:${connectionId}` : 'local'
+    const providerKey =
+      typeof connectionId === 'string'
+        ? toSshExecutionHostId(connectionId)
+        : LOCAL_EXECUTION_HOST_ID
     const livenessObservationAtStart = this.ptyLivenessObservationSequence
     if (connectionId === undefined) {
       this.ptyControllerAggregateInventoryGeneration = inventoryGeneration
diff --git a/src/main/runtime/orca-runtime-register-pty.ts b/src/main/runtime/orca-runtime-register-pty.ts
index dae2519ca9f..2d36a18a1e0 100644
--- a/src/main/runtime/orca-runtime-register-pty.ts
+++ b/src/main/runtime/orca-runtime-register-pty.ts
@@ -26,6 +26,7 @@ export class OrcaRuntimeWithRegisterPty extends OrcaRuntimeWithInvalidateAllHand
     isWsl?: boolean
   ): void {
     this.assertPtyDidNotExitBeforeRegistration(ptyId, binding?.incarnationId)
+    this.invalidatePtyControllerInventoryForLifecycle(ptyId, connectionId)
     const existingPty = this.ptysById.get(ptyId)
     const replacementHandle = binding?.terminalHandle?.trim()
     const pendingReplacement = this.pendingPtyHandleReplacementFences.get(ptyId)