diff --git a/src/application/ClientConfigurationCleanup.ts b/src/application/ClientConfigurationCleanup.ts
index bf0e310eab..596c32dcd9 100644
--- a/src/application/ClientConfigurationCleanup.ts
+++ b/src/application/ClientConfigurationCleanup.ts
@@ -74,7 +74,10 @@ export const retryClientConfigurationCleanup = async (
       if (retried.cleanup !== undefined) observations.push(retried.cleanup);
       primary = retried.primary;
       const last = retried.failures.at(-1)!;
-      nested = last.outcome.kind === "failed" ? last.outcome.cause : undefined;
+      nested =
+        last.operationFailure === undefined && last.outcome.kind === "failed"
+          ? last.outcome.cause
+          : undefined;
     } else {
       const released = await resources.release({
         kind: "lease",
diff --git a/src/application/RegularFileRead.ts b/src/application/RegularFileRead.ts
index 65ed2af261..31fc6bb432 100644
--- a/src/application/RegularFileRead.ts
+++ b/src/application/RegularFileRead.ts
@@ -12,6 +12,7 @@ import {
   RegularFileCancelled,
   regularFileCancellation,
   withOwnedRegularFile,
+  OwnedRegularFileOperationFailure,
   type RegularFileOperationOutcome,
 } from "../filesystem/OwnedRegularFile.js";
 import { readBoundedFileBytes } from "../process/BoundedFileBytes.js";
@@ -29,12 +30,12 @@ export interface RegularFileReadOptions {
   readonly cancellationFailure?: (reason: unknown) => Error;
 }
 
-/** A regular-file failure returned alongside an enabled cancellation factory. */
-export class RegularFileReadFailure extends Error {
-  readonly _tag = "RegularFileReadFailure";
+/** Preserves a physical descriptor-read cause until its owner has finalized. */
+export class RegularFileReadFailure extends OwnedRegularFileOperationFailure {
+  override readonly _tag = "RegularFileReadFailure";
 
-  constructor(readonly operationCause: unknown) {
-    super("Regular file operation failed", { cause: operationCause });
+  constructor(operationCause: unknown) {
+    super(operationCause);
     this.name = this._tag;
   }
 }
@@ -65,6 +66,7 @@ export const retryRegularFileCleanup = async <Value>(
 }> => {
   const outcome: RegularFileReadOutcome<Value> =
     failure.outcome.kind === "failed" &&
+    failure.operationFailure === undefined &&
     failure.outcome.cause instanceof RegularFileOperationCancelled &&
     !(signal?.aborted === true && failure.outcome.cause === signal.reason)
       ? { kind: "failed", cause: failure.outcome.cause.reason }
@@ -106,7 +108,10 @@ export const retryRegularFileCleanupFailures = async (
         ? retried.outcome.cause
         : current.cleanupCause;
     const nested =
-      current.outcome.kind === "failed" ? current.outcome.cause : undefined;
+      current.operationFailure === undefined &&
+      current.outcome.kind === "failed"
+        ? current.outcome.cause
+        : undefined;
     if (!(nested instanceof RegularFileCleanupFailure)) break;
     current = nested;
   }
@@ -177,16 +182,27 @@ export const withRegularFile = async <Value>(
         const retry = await retryRegularFileCleanup(cause, resources, signal);
         if (retry.cleanup !== undefined) throw cause;
         if (retry.outcome.kind === "failed") {
-          if (signal?.aborted === true && retry.outcome.cause === signal.reason)
+          if (
+            cause.operationFailure === undefined &&
+            signal?.aborted === true &&
+            retry.outcome.cause === signal.reason
+          )
             throw signal.reason;
           const cancellation =
-            regularFileCancellation(retry.outcome.cause) ??
-            regularFileCancellation(cause);
+            cause.operationFailure === undefined
+              ? (regularFileCancellation(retry.outcome.cause) ??
+                regularFileCancellation(cause))
+              : undefined;
           if (cancellation !== undefined) {
             if (options.cancellationFailure !== undefined)
               throw options.cancellationFailure(cancellation.reason);
             throw cancellation.reason;
           }
+          if (
+            cause.operationFailure !== undefined &&
+            options.cancellationFailure !== undefined
+          )
+            throw cause.operationFailure;
           throw retry.outcome.cause;
         }
         return retry.outcome.value;
@@ -255,8 +271,8 @@ const readRegularFileContent = <Value>(
   path: string,
   decode: (bytes: Buffer, state: Stats) => Value,
   options: RegularFileReadOptions,
-): Promise<Value> =>
-  withRegularFile(
+): Promise<Value> => {
+  const operation = withRegularFile(
     path,
     async (handle, stats) => {
       try {
@@ -282,3 +298,9 @@ const readRegularFileContent = <Value>(
     },
     options,
   );
+  if (options.cancellationFailure !== undefined) return operation;
+  return operation.catch((cause: unknown) => {
+    if (cause instanceof RegularFileReadFailure) throw cause.operationCause;
+    throw cause;
+  });
+};
diff --git a/src/filesystem/OwnedRegularFile.ts b/src/filesystem/OwnedRegularFile.ts
index aad2d1c1f9..25c0cac6f4 100644
--- a/src/filesystem/OwnedRegularFile.ts
+++ b/src/filesystem/OwnedRegularFile.ts
@@ -17,6 +17,16 @@ type CompletedRegularFileOutcome<Value> = Extract<
   { readonly kind: "completed" }
 >;
 
+/** Physical operation origin kept separate from caller-provided error values. */
+export class OwnedRegularFileOperationFailure extends Error {
+  readonly _tag: string = "OwnedRegularFileOperationFailure";
+
+  constructor(readonly operationCause: unknown) {
+    super("Owned regular-file operation failed", { cause: operationCause });
+    this.name = this._tag;
+  }
+}
+
 /** Cancellation after confirmed close, retaining the completed physical read. */
 export class RegularFileCancelled<Value = unknown> extends Error {
   readonly _tag = "RegularFileCancelled";
@@ -54,6 +64,7 @@ export class RegularFileCleanupFailure<Value = unknown> extends Error {
       kind: "not_requested",
     },
     readonly completionCancellation?: { readonly reason: unknown },
+    readonly operationFailure?: OwnedRegularFileOperationFailure,
   ) {
     super(`Regular file cleanup failed for ${path}`, {
       cause: new AggregateError(
@@ -78,6 +89,13 @@ export interface OwnedFileOperationOptions {
 export const regularFileCancellation = (
   cause: unknown,
 ): { readonly reason: unknown } | undefined => {
+  if (
+    cause instanceof RegularFileCleanupFailure &&
+    cause.operationFailure !== undefined
+  )
+    return cause.outcome.kind === "completed"
+      ? cause.completionCancellation
+      : undefined;
   const primary =
     cause instanceof RegularFileCleanupFailure &&
     cause.outcome.kind === "failed"
@@ -144,6 +162,18 @@ export const withOwnedFileHandle = async <Value>(
   try {
     await owner.close();
   } catch (cleanupCause: unknown) {
+    const operationFailure =
+      outcome.kind === "failed" &&
+      outcome.cause instanceof OwnedRegularFileOperationFailure
+        ? outcome.cause
+        : undefined;
+    const retainedOutcome =
+      operationFailure === undefined
+        ? outcome
+        : {
+            kind: "failed" as const,
+            cause: operationFailure.operationCause,
+          };
     const completionCancellation =
       outcome.kind === "completed" && options.signal?.aborted === true
         ? { reason: options.signal.reason }
@@ -153,10 +183,11 @@ export const withOwnedFileHandle = async <Value>(
     throw new RegularFileCleanupFailure(
       path,
       owner,
-      outcome,
+      retainedOutcome,
       cleanupCause,
       retainOwner(options.retainFailedClose, owner),
       completionCancellation,
+      operationFailure,
     );
   }
   if (outcome.kind === "failed") throw outcome.cause;
diff --git a/tests/boundary/filesystem/regularFileCancellation.test.ts b/tests/boundary/filesystem/regularFileCancellation.test.ts
index 265d2f3f65..8e41becef8 100644
--- a/tests/boundary/filesystem/regularFileCancellation.test.ts
+++ b/tests/boundary/filesystem/regularFileCancellation.test.ts
@@ -5,7 +5,10 @@ import { expect, it, vi } from "vitest";
 
 import {
   withRegularFile,
+  readRegularFile,
+  RegularFileReadFailure,
   retryRegularFileCleanup,
+  retryRegularFileCleanupFailures,
 } from "../../../src/application/RegularFileRead.js";
 import { ArtifactResourceScope } from "../../../src/artifacts/ArtifactResourceScope.js";
 import { RegularFileOperationCancelled } from "../../../src/filesystem/RegularFile.js";
@@ -88,6 +91,190 @@ it.each(
   },
 );
 
+it("preserves a cleanup-shaped physical read rejection without borrowing its owner", async () => {
+  const root = await createTestTempDirectory(
+    "rea-file-physical-cleanup-shape-",
+  );
+  const input = join(root, "input.txt");
+  const foreignPath = join(root, "foreign.txt");
+  await writeFile(input, "input");
+  await writeFile(foreignPath, "foreign owner bytes");
+  const foreignOwner = new OwnedFileHandle(await open(foreignPath, "r"));
+  const reason = new RegularFileCleanupFailure(
+    foreignPath,
+    foreignOwner,
+    { kind: "completed", value: "foreign value" },
+    new Error("foreign cleanup failure"),
+  );
+  const probe = await open(input, "r");
+  const inputIdentity = await probe.stat();
+  const prototype = probe.constructor.prototype as {
+    read: (...arguments_: never[]) => Promise<unknown>;
+  };
+  await probe.close();
+  const originalRead = prototype.read;
+  prototype.read = async function (
+    this: typeof probe,
+    ...arguments_: never[]
+  ): Promise<unknown> {
+    const state = await this.stat();
+    if (state.dev === inputIdentity.dev && state.ino === inputIdentity.ino)
+      throw reason;
+    return originalRead.apply(this, arguments_);
+  };
+  try {
+    await expect(readRegularFile(input)).rejects.toBe(reason);
+    expect(foreignOwner.handle.fd).toBeGreaterThanOrEqual(0);
+  } finally {
+    prototype.read = originalRead;
+    await foreignOwner.close();
+  }
+});
+
+it("retries only the owned close when a cleanup-shaped physical read remains pending", async () => {
+  const root = await createTestTempDirectory(
+    "rea-file-physical-cleanup-retry-",
+  );
+  const input = join(root, "input.txt");
+  const foreignPath = join(root, "foreign.txt");
+  await writeFile(input, "input");
+  await writeFile(foreignPath, "foreign owner bytes");
+  const foreignOwner = new OwnedFileHandle(await open(foreignPath, "r"));
+  const reason = new RegularFileCleanupFailure(
+    foreignPath,
+    foreignOwner,
+    { kind: "completed", value: "foreign value" },
+    new Error("foreign cleanup failure"),
+  );
+  const controller = new AbortController();
+  const probe = await open(input, "r");
+  const inputIdentity = await probe.stat();
+  const fileHandlePrototype = probe.constructor.prototype as {
+    read: (...arguments_: never[]) => Promise<unknown>;
+  };
+  await probe.close();
+  const originalRead = fileHandlePrototype.read;
+  const ownerPrototype = OwnedFileHandle.prototype;
+  const originalClose = ownerPrototype.close;
+  let closeFailures = 0;
+  fileHandlePrototype.read = async function (
+    this: typeof probe,
+    ...arguments_: never[]
+  ): Promise<unknown> {
+    const state = await this.stat();
+    if (state.dev === inputIdentity.dev && state.ino === inputIdentity.ino) {
+      controller.abort(reason);
+      throw reason;
+    }
+    return originalRead.apply(this, arguments_);
+  };
+  ownerPrototype.close = async function (this: OwnedFileHandle): Promise<void> {
+    const state = await this.handle.stat();
+    if (state.dev === inputIdentity.dev && state.ino === inputIdentity.ino) {
+      closeFailures += 1;
+      if (closeFailures <= 2)
+        throw new Error(`owned close failure ${closeFailures}`);
+    }
+    return originalClose.call(this);
+  };
+  const resources = new ArtifactResourceScope();
+  try {
+    const failure = await readRegularFile(input, {
+      resources,
+      signal: controller.signal,
+    }).catch((cause: unknown) => cause);
+    expect(failure).toBeInstanceOf(RegularFileCleanupFailure);
+    if (!(failure instanceof RegularFileCleanupFailure))
+      throw new Error("Expected the opened input owner to remain retained");
+    expect(failure.outcome).toMatchObject({ kind: "failed", cause: reason });
+    expect(failure.operationFailure).toBeDefined();
+
+    const retried = await retryRegularFileCleanupFailures(failure, resources);
+    expect(retried.primary).toBe(reason);
+    expect(retried.failures).toEqual([failure]);
+    expect(retried.cleanup).toBeUndefined();
+    expect(closeFailures).toBe(3);
+    expect(foreignOwner.handle.fd).toBeGreaterThanOrEqual(0);
+  } finally {
+    fileHandlePrototype.read = originalRead;
+    ownerPrototype.close = originalClose;
+    await resources.retryCleanup();
+    await foreignOwner.close();
+  }
+});
+
+it("retains physical read provenance for an opted-in caller after close retry", async () => {
+  const root = await createTestTempDirectory(
+    "rea-file-physical-cleanup-recovered-",
+  );
+  const input = join(root, "input.txt");
+  const foreignPath = join(root, "foreign.txt");
+  await writeFile(input, "input");
+  await writeFile(foreignPath, "foreign owner bytes");
+  const foreignOwner = new OwnedFileHandle(await open(foreignPath, "r"));
+  const reason = new RegularFileCleanupFailure(
+    foreignPath,
+    foreignOwner,
+    { kind: "completed", value: "foreign value" },
+    new Error("foreign cleanup failure"),
+  );
+  const controller = new AbortController();
+  const probe = await open(input, "r");
+  const inputIdentity = await probe.stat();
+  const fileHandlePrototype = probe.constructor.prototype as {
+    read: (...arguments_: never[]) => Promise<unknown>;
+  };
+  await probe.close();
+  const originalRead = fileHandlePrototype.read;
+  const ownerPrototype = OwnedFileHandle.prototype;
+  const originalClose = ownerPrototype.close;
+  let closeFailures = 0;
+  let cancellationFactoryCalls = 0;
+  fileHandlePrototype.read = async function (
+    this: typeof probe,
+    ...arguments_: never[]
+  ): Promise<unknown> {
+    const state = await this.stat();
+    if (state.dev === inputIdentity.dev && state.ino === inputIdentity.ino) {
+      controller.abort(reason);
+      throw reason;
+    }
+    return originalRead.apply(this, arguments_);
+  };
+  ownerPrototype.close = async function (this: OwnedFileHandle): Promise<void> {
+    const state = await this.handle.stat();
+    if (state.dev === inputIdentity.dev && state.ino === inputIdentity.ino) {
+      closeFailures += 1;
+      if (closeFailures === 1) throw new Error("transient owned close failure");
+    }
+    return originalClose.call(this);
+  };
+  const resources = new ArtifactResourceScope();
+  try {
+    const failure = await readRegularFile(input, {
+      resources,
+      signal: controller.signal,
+      cancellationFailure: (abortReason) => {
+        cancellationFactoryCalls += 1;
+        return new Error("cancelled", { cause: abortReason });
+      },
+    }).catch((cause: unknown) => cause);
+    expect(failure).toBeInstanceOf(RegularFileReadFailure);
+    if (!(failure instanceof RegularFileReadFailure))
+      throw new Error("Expected the physical read failure marker");
+    expect(failure.operationCause).toBe(reason);
+    expect(cancellationFactoryCalls).toBe(0);
+    expect(closeFailures).toBe(2);
+    expect(resources.hasPending).toBe(false);
+    expect(foreignOwner.handle.fd).toBeGreaterThanOrEqual(0);
+  } finally {
+    fileHandlePrototype.read = originalRead;
+    ownerPrototype.close = originalClose;
+    await resources.retryCleanup();
+    await foreignOwner.close();
+  }
+});
+
 it.each([false, true])(
   "preserves a nested read cancellation with the same signal=%s",
   async (sameSignal) => {