diff --git a/src/artifacts/DirectoryArtifactReader.ts b/src/artifacts/DirectoryArtifactReader.ts
index 123a1cb092..69beb8e1d1 100644
--- a/src/artifacts/DirectoryArtifactReader.ts
+++ b/src/artifacts/DirectoryArtifactReader.ts
@@ -1,23 +1,32 @@
-import { constants } from "node:fs";
-import { lstat, open, opendir, realpath } from "node:fs/promises";
+import { constants, type Dir, type Stats } from "node:fs";
+import {
+  lstat,
+  open,
+  opendir,
+  realpath,
+  type FileHandle,
+} from "node:fs/promises";
 import { isAbsolute, join, relative, sep } from "node:path";
-import type { Readable } from "node:stream";
+import { Readable } from "node:stream";
 
 import {
   ArtifactReaderFailure,
   type ArtifactEntry,
   type ArtifactReader,
 } from "./ArtifactReader.js";
+import { OwnedFileHandle } from "../filesystem/OwnedFileHandle.js";
+import { readFileHandleChunks } from "../filesystem/readFileHandleChunks.js";
 
 /** Non-symlink-following directory reader. */
 export class DirectoryArtifactReader implements ArtifactReader {
   readonly format = "directory" as const;
-  readonly #rootPromise: Promise<string>;
+  #rootPromise: Promise<string> | undefined;
   readonly #rootPath: string;
+  readonly #directories = new Set<OwnedDirectoryHandle>();
+  readonly #files = new Map<OwnedFileHandle, string>();
 
   constructor(root: string) {
     this.#rootPath = root;
-    this.#rootPromise = realpath(root);
   }
 
   /** Enumerate entries, optionally restricting descent while retaining directories. */
@@ -25,9 +34,7 @@ export class DirectoryArtifactReader implements ArtifactReader {
     signal?: AbortSignal,
     descendInto?: (path: string) => boolean,
   ): AsyncIterable<ArtifactEntry> {
-    const root = await this.#rootPromise.catch((cause: unknown) => {
-      throw directoryIoFailure("resolve artifact root", this.#rootPath, cause);
-    });
+    const root = await this.#resolveRoot();
     const pending = [root];
     while (pending.length > 0) {
       abortIfNeeded(signal);
@@ -36,62 +43,100 @@ export class DirectoryArtifactReader implements ArtifactReader {
       await withDirectoryIoContext("inspect directory", directory, () =>
         assertContainedDirectory(root, directory),
       );
-      const handle = await opendir(directory).catch((cause: unknown) => {
-        throw directoryIoFailure("open directory", directory, cause);
-      });
-      const directories: string[] = [];
-      try {
-        for await (const child of handle) {
-          abortIfNeeded(signal);
-          const absolute = join(directory, child.name);
-          const metadata = await lstat(absolute).catch((cause: unknown) => {
-            throw directoryIoFailure("inspect entry", absolute, cause);
-          });
-          const path = relative(root, absolute).split(sep).join("/");
-          const kind = metadata.isSymbolicLink()
-            ? "symlink"
-            : metadata.isDirectory()
-              ? "directory"
-              : metadata.isFile()
-                ? "file"
-                : undefined;
-          if (kind === undefined) continue;
-          yield {
-            path,
-            kind,
-            declaredSize: kind === "file" ? metadata.size : null,
-            compressedSize: null,
-            executable: (metadata.mode & 0o111) !== 0,
-            encrypted: false,
-            byteOffset: null,
-            declaredSha256: null,
-            unpacked: false,
-            limitations:
-              kind === "symlink"
-                ? ["Symlink target was not followed or disclosed."]
-                : [],
-            adapterKey: absolute,
-            ...(kind === "file"
-              ? {
-                  sourceIdentity: { device: metadata.dev, inode: metadata.ino },
-                }
-              : {}),
-          };
-          if (kind === "directory" && (descendInto?.(path) ?? true))
-            directories.push(absolute);
-        }
-      } catch (cause: unknown) {
-        if (cause instanceof ArtifactReaderFailure) throw cause;
-        throw directoryIoFailure("read directory", directory, cause);
-      } finally {
-        // best-effort cleanup: directory-handle close must not mask traversal.
-        await handle.close().catch(() => undefined);
-      }
+      for await (const entry of this.#readDirectory(
+        directory,
+        pending,
+        signal,
+        descendInto,
+      ))
+        yield entry;
       await withDirectoryIoContext("inspect directory", directory, () =>
         assertContainedDirectory(root, directory),
       );
-      directories.reverse();
-      pending.push(...directories);
+    }
+  }
+
+  async #resolveRoot(): Promise<string> {
+    return (this.#rootPromise ??= realpath(this.#rootPath)).catch(
+      (cause: unknown) => {
+        throw directoryIoFailure(
+          "resolve artifact root",
+          this.#rootPath,
+          cause,
+        );
+      },
+    );
+  }
+
+  async *#readDirectory(
+    directory: string,
+    pending: string[],
+    signal?: AbortSignal,
+    descendInto?: (path: string) => boolean,
+  ): AsyncIterable<ArtifactEntry> {
+    const root = await this.#resolveRoot();
+    const handle = new OwnedDirectoryHandle(
+      await opendir(directory).catch((cause: unknown) => {
+        throw directoryIoFailure("open directory", directory, cause);
+      }),
+    );
+    this.#directories.add(handle);
+    const childDirectories: string[] = [];
+    let traversal:
+      | { readonly kind: "complete" }
+      | { readonly kind: "failed"; readonly cause: unknown } = {
+      kind: "complete",
+    };
+    try {
+      for (;;) {
+        const child = await handle.handle.read();
+        if (child === null) break;
+        abortIfNeeded(signal);
+        const absolute = join(directory, child.name);
+        const metadata = await lstat(absolute).catch((cause: unknown) => {
+          throw directoryIoFailure("inspect entry", absolute, cause);
+        });
+        const path = relative(root, absolute).split(sep).join("/");
+        const entry = artifactEntry(path, absolute, metadata);
+        if (entry === undefined) continue;
+        yield entry;
+        if (entry.kind === "directory" && (descendInto?.(path) ?? true))
+          childDirectories.push(absolute);
+      }
+    } catch (cause: unknown) {
+      traversal = {
+        kind: "failed",
+        cause:
+          cause instanceof ArtifactReaderFailure
+            ? cause
+            : directoryIoFailure("read directory", directory, cause),
+      };
+    } finally {
+      await this.#finishDirectory(handle, directory, traversal);
+    }
+    if (traversal.kind === "failed") throw traversal.cause;
+    childDirectories.reverse();
+    pending.push(...childDirectories);
+  }
+
+  async #finishDirectory(
+    handle: OwnedDirectoryHandle,
+    path: string,
+    traversal:
+      | { readonly kind: "complete" }
+      | { readonly kind: "failed"; readonly cause: unknown },
+  ): Promise<void> {
+    try {
+      await handle.close();
+      this.#directories.delete(handle);
+    } catch (cause: unknown) {
+      const closeFailure = directoryIoFailure("close directory", path, cause);
+      if (traversal.kind === "failed")
+        throw ArtifactReaderFailure.withCleanup(
+          traversal.cause,
+          ArtifactReaderFailure.cleanupObservation(closeFailure, path),
+        );
+      throw closeFailure;
     }
   }
 
@@ -102,14 +147,16 @@ export class DirectoryArtifactReader implements ArtifactReader {
         "format",
         "Only regular files can be opened",
       );
-    const handle = await open(
+    const fileHandle = await open(
       entry.adapterKey,
       constants.O_RDONLY | constants.O_NOFOLLOW | constants.O_NONBLOCK,
     ).catch((cause: unknown) => {
       throw directoryIoFailure("open entry", entry.adapterKey, cause);
     });
+    const owner = new OwnedFileHandle(fileHandle);
+    this.#files.set(owner, entry.adapterKey);
     try {
-      const observed = await handle.stat().catch((cause: unknown) => {
+      const observed = await owner.handle.stat().catch((cause: unknown) => {
         throw directoryIoFailure(
           "inspect opened entry",
           entry.adapterKey,
@@ -127,16 +174,76 @@ export class DirectoryArtifactReader implements ArtifactReader {
           `Directory entry changed before open: ${entry.path}`,
         );
       }
-      return handle.createReadStream({ autoClose: true });
+      abortIfNeeded(signal);
+      const source = Readable.from(
+        mapFileReadCancellation(owner.handle, signal),
+        { objectMode: false },
+      );
+      source.once("close", () => {
+        void this.#closeFile(owner).catch(() => undefined);
+      });
+      return source;
     } catch (cause: unknown) {
-      // best-effort cleanup: file-handle close must not mask the open failure.
-      await handle.close().catch(() => undefined);
+      try {
+        await this.#closeFile(owner);
+      } catch (closeCause: unknown) {
+        throw ArtifactReaderFailure.withCleanup(
+          cause,
+          ArtifactReaderFailure.cleanupObservation(
+            directoryIoFailure(
+              "close opened entry",
+              entry.adapterKey,
+              closeCause,
+            ),
+            entry.adapterKey,
+          ),
+        );
+      }
       throw cause;
     }
   }
 
-  close(): Promise<void> {
-    return Promise.resolve();
+  async close(): Promise<void> {
+    const failures: unknown[] = [];
+    for (const [owner, path] of this.#files) {
+      try {
+        await this.#closeFile(owner);
+      } catch (cause: unknown) {
+        failures.push(directoryIoFailure("close opened entry", path, cause));
+      }
+    }
+    for (const owner of this.#directories) {
+      try {
+        await owner.close();
+        this.#directories.delete(owner);
+      } catch (cause: unknown) {
+        failures.push(
+          directoryIoFailure("close directory", owner.handle.path, cause),
+        );
+      }
+    }
+    if (failures.length > 0) {
+      const reason = failures.map(failureMessage).join("; ");
+      throw new ArtifactReaderFailure(
+        "io",
+        `Directory artifact cleanup failed: ${reason}`,
+        {
+          cause: new AggregateError(failures),
+          cleanup: {
+            reason,
+            resources: [
+              ...this.#files.values(),
+              ...[...this.#directories].map((owner) => owner.handle.path),
+            ],
+          },
+        },
+      );
+    }
+  }
+
+  async #closeFile(owner: OwnedFileHandle<FileHandle>): Promise<void> {
+    await owner.close();
+    this.#files.delete(owner);
   }
 
   provenance(): readonly [] {
@@ -144,6 +251,74 @@ export class DirectoryArtifactReader implements ArtifactReader {
   }
 }
 
+const artifactEntry = (
+  path: string,
+  absolute: string,
+  metadata: Stats,
+): ArtifactEntry | undefined => {
+  const kind = metadata.isSymbolicLink()
+    ? "symlink"
+    : metadata.isDirectory()
+      ? "directory"
+      : metadata.isFile()
+        ? "file"
+        : undefined;
+  if (kind === undefined) return undefined;
+  return {
+    path,
+    kind,
+    declaredSize: kind === "file" ? metadata.size : null,
+    compressedSize: null,
+    executable: (metadata.mode & 0o111) !== 0,
+    encrypted: false,
+    byteOffset: null,
+    declaredSha256: null,
+    unpacked: false,
+    limitations:
+      kind === "symlink"
+        ? ["Symlink target was not followed or disclosed."]
+        : [],
+    adapterKey: absolute,
+    ...(kind === "file"
+      ? {
+          sourceIdentity: { device: metadata.dev, inode: metadata.ino },
+        }
+      : {}),
+  };
+};
+
+type DirectoryCloseState =
+  | { readonly kind: "open" }
+  | { readonly kind: "closing"; readonly attempt: Promise<void> }
+  | { readonly kind: "closed" }
+  | { readonly kind: "failed"; readonly cause: unknown };
+
+/** Dir.close invalidates Node's private handle before its native close settles. */
+class OwnedDirectoryHandle {
+  #state: DirectoryCloseState = { kind: "open" };
+
+  constructor(readonly handle: Dir) {}
+
+  close(): Promise<void> {
+    if (this.#state.kind === "closed") return Promise.resolve();
+    if (this.#state.kind === "closing") return this.#state.attempt;
+    if (this.#state.kind === "failed") return Promise.reject(this.#state.cause);
+    const attempt = Promise.resolve().then(async () => {
+      try {
+        await this.handle.close();
+        this.#state = { kind: "closed" };
+      } catch (cause: unknown) {
+        // Dir exposes no public validity signal; a second close can only lie
+        // with ERR_DIR_CLOSED after Node has invalidated the first owner.
+        this.#state = { kind: "failed", cause };
+        throw cause;
+      }
+    });
+    this.#state = { kind: "closing", attempt };
+    return attempt;
+  }
+}
+
 const directoryIoFailure = (
   operation: string,
   path: string,
@@ -157,13 +332,38 @@ const directoryIoFailure = (
     typeof cause.code === "string"
       ? ` (${cause.code})`
       : "";
+  const detail = failureMessage(cause);
   return new ArtifactReaderFailure(
     "io",
-    `Could not ${operation} at ${path}${code}`,
+    `Could not ${operation} at ${path}${code}: ${detail}`,
     { cause },
   );
 };
 
+const failureMessage = (cause: unknown): string =>
+  cause instanceof Error ? cause.message : String(cause);
+
+const mapFileReadCancellation = async function* (
+  handle: FileHandle,
+  signal?: AbortSignal,
+): AsyncGenerator<Buffer> {
+  try {
+    for await (const chunk of readFileHandleChunks(handle, { signal })) {
+      abortIfNeeded(signal);
+      yield chunk;
+    }
+    abortIfNeeded(signal);
+  } catch (cause: unknown) {
+    if (signal?.aborted === true)
+      throw new ArtifactReaderFailure(
+        "cancelled",
+        "Directory artifact read cancelled",
+        { cause },
+      );
+    throw cause;
+  }
+};
+
 const withDirectoryIoContext = async <T>(
   operation: string,
   path: string,
diff --git a/src/artifacts/MachOSliceArtifactReader.ts b/src/artifacts/MachOSliceArtifactReader.ts
index 540fe17263..e21e975549 100644
--- a/src/artifacts/MachOSliceArtifactReader.ts
+++ b/src/artifacts/MachOSliceArtifactReader.ts
@@ -12,6 +12,7 @@ import {
   type LipoArchitecture,
 } from "../native/parsers/lipo.js";
 import type { MachoSlice } from "../domain/apple/dylibResolution.js";
+import { OwnedFileHandle } from "../filesystem/OwnedFileHandle.js";
 import { readMachoImage, type ReadAt } from "./apple/MachoLoadCommandReader.js";
 import {
   ArtifactReaderFailure,
@@ -22,6 +23,8 @@ import {
 } from "./ArtifactReader.js";
 import { streamChunkToBuffer } from "./StreamBytes.js";
 import {
+  NonRegularFileReadError,
+  RegularFileAdmissionFailure,
   openRegularFile,
   sameRegularFileState,
   type StableRegularFileDescriptor,
@@ -33,6 +36,7 @@ export class MachOSliceArtifactReader implements ArtifactReader {
   readonly format = "file" as const;
   #command: ArtifactCommand | undefined;
   #source: StableRegularFileDescriptor | undefined;
+  #ownedSource: OwnedFileHandle | undefined;
   #pendingSource: Promise<StableRegularFileDescriptor> | undefined;
   readonly #entries = new Map<string, ArtifactEntry>();
   readonly #ownsSource: boolean;
@@ -283,23 +287,51 @@ export class MachOSliceArtifactReader implements ArtifactReader {
   }
 
   async #acquireSource(): Promise<StableRegularFileDescriptor> {
-    const handle = await openRegularFile(this.path, { symlinks: "reject" });
+    let handle: FileHandle;
+    try {
+      handle = await openRegularFile(this.path, { symlinks: "reject" });
+    } catch (cause: unknown) {
+      if (!(cause instanceof RegularFileAdmissionFailure)) throw cause;
+      this.#ownedSource = cause.owner;
+      const primary =
+        cause.cause instanceof NonRegularFileReadError
+          ? new ArtifactReaderFailure(
+              "format",
+              `Universal Mach-O source is not a regular file: ${this.path}`,
+              { cause: cause.cause },
+            )
+          : cause.cause;
+      throw ArtifactReaderFailure.withCleanup(
+        primary,
+        ArtifactReaderFailure.cleanupObservation(cause.cleanupCause, this.path),
+      );
+    }
+    const owner = new OwnedFileHandle(handle);
+    this.#ownedSource = owner;
     try {
       const initial = await handle.stat();
       const source = { handle, initial };
       this.#source = source;
       return source;
     } catch (cause: unknown) {
-      await handle.close().catch(() => undefined);
+      try {
+        await owner.close();
+        this.#ownedSource = undefined;
+      } catch (cleanupCause: unknown) {
+        throw ArtifactReaderFailure.withCleanup(
+          cause,
+          ArtifactReaderFailure.cleanupObservation(cleanupCause, this.path),
+        );
+      }
       throw cause;
     }
   }
 
   async #closeSource(): Promise<void> {
     await this.#pendingSource?.catch(() => undefined);
-    if (!this.#ownsSource || this.#source === undefined) return;
-    const source = this.#source;
-    await source.handle.close();
+    if (!this.#ownsSource || this.#ownedSource === undefined) return;
+    await this.#ownedSource.close();
+    this.#ownedSource = undefined;
     this.#source = undefined;
   }
 
diff --git a/src/artifacts/ZipArtifactReader.ts b/src/artifacts/ZipArtifactReader.ts
index ca3988a70d..fbffd76d8d 100644
--- a/src/artifacts/ZipArtifactReader.ts
+++ b/src/artifacts/ZipArtifactReader.ts
@@ -12,8 +12,10 @@ import {
   type ArtifactReader,
 } from "./ArtifactReader.js";
 import type { ZipPackageFormat } from "../domain/zipPackageFormat.js";
+import { OwnedFileHandle } from "../filesystem/OwnedFileHandle.js";
 import {
   NonRegularFileReadError,
+  RegularFileAdmissionFailure,
   openRegularFile,
   sameRegularFileState,
   type StableRegularFileDescriptor,
@@ -21,6 +23,7 @@ import {
 
 class NodeFileReader extends Reader<string> {
   #handle: FileHandle | undefined;
+  #owner: OwnedFileHandle | undefined;
   #initPromise: Promise<void> | undefined;
   readonly #ownsHandle: boolean;
 
@@ -40,10 +43,30 @@ class NodeFileReader extends Reader<string> {
 
   async #initialize(): Promise<void> {
     try {
-      this.#handle =
+      const handle =
         this.admitted?.handle ??
         (await openRegularFile(this.path, { symlinks: "reject" }));
+      this.#handle = handle;
+      if (this.#ownsHandle) this.#owner = new OwnedFileHandle(handle);
     } catch (cause: unknown) {
+      if (cause instanceof RegularFileAdmissionFailure) {
+        this.#owner = cause.owner;
+        const primary =
+          cause.cause instanceof NonRegularFileReadError
+            ? new ArtifactReaderFailure(
+                "format",
+                `ZIP source is not a regular file: ${this.path}`,
+                { cause: cause.cause },
+              )
+            : cause.cause;
+        throw ArtifactReaderFailure.withCleanup(
+          primary,
+          ArtifactReaderFailure.cleanupObservation(
+            cause.cleanupCause,
+            this.path,
+          ),
+        );
+      }
       if (cause instanceof NonRegularFileReadError)
         throw new ArtifactReaderFailure(
           "format",
@@ -88,8 +111,9 @@ class NodeFileReader extends Reader<string> {
   async closeHandle(): Promise<void> {
     if (!this.#ownsHandle) return;
     await this.#initPromise?.catch(() => undefined);
-    if (this.#handle === undefined) return;
-    await this.#handle.close();
+    if (this.#owner === undefined) return;
+    await this.#owner.close();
+    this.#owner = undefined;
     this.#handle = undefined;
   }
 }
diff --git a/tests/boundary/filesystem/directoryArtifactReaderFifoRace.test.ts b/tests/boundary/filesystem/directoryArtifactReaderFifoRace.test.ts
index 443de83f20..7e504bd22a 100644
--- a/tests/boundary/filesystem/directoryArtifactReaderFifoRace.test.ts
+++ b/tests/boundary/filesystem/directoryArtifactReaderFifoRace.test.ts
@@ -1,7 +1,9 @@
+import { execFile } from "node:child_process";
 import { writeFile } from "node:fs/promises";
 import { tmpdir } from "node:os";
 import { join } from "node:path";
 import { randomUUID } from "node:crypto";
+import { promisify } from "node:util";
 import { fileURLToPath } from "node:url";
 
 import { expect, it } from "vitest";
@@ -12,6 +14,8 @@ import {
 } from "../../../src/process/ProviderProcess.js";
 import { createTestTempDirectory } from "../../fixtures/temporaryDirectory.js";
 
+const run = promisify(execFile);
+
 it.skipIf(process.platform === "win32")(
   "rejects a FIFO replacement without blocking the owner process",
   async () => {
@@ -51,3 +55,46 @@ it.skipIf(process.platform === "win32")(
     }
   },
 );
+
+it.skipIf(process.platform === "win32")(
+  "skips unsupported FIFO entries and continues through the directory",
+  async () => {
+    const root = await createTestTempDirectory("rea-directory-entry-fifo-");
+    await writeFile(join(root, "module.js"), "export {}\n");
+    await run("mkfifo", [join(root, "unsupported.fifo")]);
+    const probe = fileURLToPath(
+      new URL(
+        "../../fixtures/directoryReaderUnsupportedEntryProbe.mjs",
+        import.meta.url,
+      ),
+    );
+    const readerModule = fileURLToPath(
+      new URL(
+        "../../../dist/artifacts/DirectoryArtifactReader.js",
+        import.meta.url,
+      ),
+    );
+    const launch = await spawnOwnedProviderProcess({
+      command: process.execPath,
+      arguments: [probe, readerModule, root],
+      runId: `rea-directory-entry-fifo-${randomUUID()}`,
+      cwd: tmpdir(),
+      hostEnvironment: process.env,
+    });
+    const supervisor = new ProviderProcessSupervisor({
+      ...launch,
+      ownsProcessLifetime: true,
+    });
+
+    try {
+      expect(await supervisor.waitForOutputClose(2_000)).toBe(true);
+      expect(supervisor.snapshot().stdout.text.trim()).toBe('["module.js"]');
+    } finally {
+      const stopped = await supervisor.stop({
+        terminationGraceMs: 100,
+        killGraceMs: 500,
+      });
+      expect(stopped.status).not.toBe("incomplete");
+    }
+  },
+);
diff --git a/tests/boundary/filesystem/directoryArtifactReaderOwnership.test.ts b/tests/boundary/filesystem/directoryArtifactReaderOwnership.test.ts
new file mode 100644
index 0000000000..4145e7bca2
--- /dev/null
+++ b/tests/boundary/filesystem/directoryArtifactReaderOwnership.test.ts
@@ -0,0 +1,216 @@
+import { writeFile, type FileHandle } from "node:fs/promises";
+import { join } from "node:path";
+
+import { afterEach, describe, expect, it, vi } from "vitest";
+
+const controls = vi.hoisted(() => ({
+  wrapDirectory: undefined as
+    | ((handle: { close(): Promise<void>; readonly path: string }) => void)
+    | undefined,
+  wrapFile: undefined as
+    | ((handle: { close(): Promise<void>; readonly fd: number }) => void)
+    | undefined,
+}));
+
+vi.mock("node:fs/promises", async (importOriginal) => {
+  const actual = await importOriginal<typeof import("node:fs/promises")>();
+  return {
+    ...actual,
+    opendir: async (...args: Parameters<typeof actual.opendir>) => {
+      const handle = await actual.opendir(...args);
+      controls.wrapDirectory?.(handle);
+      return handle;
+    },
+    open: async (...args: Parameters<typeof actual.open>) => {
+      const handle = await actual.open(...args);
+      controls.wrapFile?.(handle);
+      return handle;
+    },
+  };
+});
+
+import { ArtifactReaderFailure } from "../../../src/artifacts/ArtifactReader.js";
+import { DirectoryArtifactReader } from "../../../src/artifacts/DirectoryArtifactReader.js";
+import { createTestTempDirectory } from "../../fixtures/temporaryDirectory.js";
+
+const makeFixture = async () => {
+  const root = await createTestTempDirectory("rea-directory-owner-");
+  const file = join(root, "sample.txt");
+  await writeFile(file, "directory content\n");
+  return { root, file, reader: new DirectoryArtifactReader(root) };
+};
+
+afterEach(() => {
+  controls.wrapDirectory = undefined;
+  controls.wrapFile = undefined;
+  vi.restoreAllMocks();
+});
+
+describe("DirectoryArtifactReader resource ownership", () => {
+  it("closes the exact directory owner on early iterator return", async () => {
+    const { reader } = await makeFixture();
+    let closeCalls = 0;
+    controls.wrapDirectory = (handle) => {
+      const close = handle.close.bind(handle);
+      handle.close = async () => {
+        closeCalls += 1;
+        await close();
+      };
+    };
+
+    try {
+      const entries = reader.entries()[Symbol.asyncIterator]();
+      expect((await entries.next()).done).toBe(false);
+      await entries.return?.();
+      expect(closeCalls).toBe(1);
+      await reader.close();
+      expect(closeCalls).toBe(1);
+    } finally {
+      await reader.close();
+    }
+  });
+
+  it("retains an invalidated directory owner after native close rejection", async () => {
+    const { reader } = await makeFixture();
+    const nativeFailure = new Error("injected native directory close failure");
+    let closeCalls = 0;
+    controls.wrapDirectory = (handle) => {
+      const close = handle.close.bind(handle);
+      handle.close = async () => {
+        closeCalls += 1;
+        await close();
+        throw nativeFailure;
+      };
+    };
+
+    try {
+      await expect(async () => {
+        for await (const _entry of reader.entries()) {
+          // Read through EOF so the explicit owner close runs.
+        }
+      }).rejects.toMatchObject({
+        reason: "io",
+        message: expect.stringContaining("close directory"),
+      });
+
+      const cleanupFailure = await reader
+        .close()
+        .catch((cause: unknown) => cause);
+      expect(cleanupFailure).toBeInstanceOf(ArtifactReaderFailure);
+      expect((cleanupFailure as Error).message).toContain("cleanup failed");
+      expect(closeCalls).toBe(1);
+      const aggregate = (cleanupFailure as Error & { cause: AggregateError })
+        .cause;
+      expect(
+        aggregate.errors.some(
+          (cause) => cause instanceof Error && cause.cause === nativeFailure,
+        ),
+      ).toBe(true);
+    } finally {
+      await reader.close().catch(() => undefined);
+    }
+  });
+
+  it("preserves cancellation while retaining a failed directory close", async () => {
+    const { root, reader } = await makeFixture();
+    await writeFile(join(root, "second.txt"), "second entry\n");
+    const closeFailure = new Error("injected close after cancellation");
+    let closeCalls = 0;
+    controls.wrapDirectory = (handle) => {
+      const close = handle.close.bind(handle);
+      handle.close = async () => {
+        closeCalls += 1;
+        await close();
+        throw closeFailure;
+      };
+    };
+
+    try {
+      const controller = new AbortController();
+      const entries = reader.entries(controller.signal)[Symbol.asyncIterator]();
+      expect((await entries.next()).done).toBe(false);
+      controller.abort();
+      const failure = await entries.next().catch((cause: unknown) => cause);
+      expect(failure).toMatchObject({ reason: "cancelled" });
+      expect((failure as ArtifactReaderFailure).cleanup?.resources).toEqual([
+        root,
+      ]);
+      expect(closeCalls).toBe(1);
+      await expect(reader.close()).rejects.toMatchObject({ reason: "io" });
+      expect(closeCalls).toBe(1);
+    } finally {
+      await reader.close().catch(() => undefined);
+    }
+  });
+});
+
+describe("DirectoryArtifactReader file handle ownership", () => {
+  it("retries an uninvalidated file close through its retained owner", async () => {
+    const { reader } = await makeFixture();
+    let fileCloseCalls = 0;
+    let openedHandle: FileHandle | undefined;
+    controls.wrapFile = (handle) => {
+      if (handle.fd < 0) return;
+      openedHandle = handle as FileHandle;
+      const close = handle.close.bind(handle);
+      handle.close = async () => {
+        fileCloseCalls += 1;
+        if (fileCloseCalls === 1) throw new Error("before native close");
+        await close();
+      };
+    };
+
+    try {
+      let entry;
+      for await (const observed of reader.entries()) {
+        if (observed.path === "sample.txt") entry = observed;
+      }
+      if (entry === undefined)
+        throw new Error("fixture file was not inventoried");
+      const stream = await reader.open(entry);
+      stream.destroy();
+      await new Promise<void>((resolve) => stream.once("close", resolve));
+      await new Promise<void>((resolve) => setImmediate(resolve));
+      expect(fileCloseCalls).toBe(1);
+      expect(openedHandle?.fd).toBeGreaterThanOrEqual(0);
+      await reader.close();
+      expect(fileCloseCalls).toBe(2);
+      expect(openedHandle?.fd).toBe(-1);
+    } finally {
+      await reader.close().catch(() => undefined);
+    }
+  });
+
+  it("maps an aborted positional read to typed cancellation and owner close", async () => {
+    const { file, reader } = await makeFixture();
+    await writeFile(file, Buffer.alloc(256 * 1024, 0x5a));
+    try {
+      let entry;
+      for await (const observed of reader.entries()) {
+        if (observed.path === "sample.txt") entry = observed;
+      }
+      if (entry === undefined)
+        throw new Error("fixture file was not inventoried");
+      const controller = new AbortController();
+      const stream = await reader.open(entry, controller.signal);
+      const closed = new Promise<void>((resolve) =>
+        stream.once("close", resolve),
+      );
+      const outcome = new Promise<unknown>((resolve, reject) => {
+        stream.once("error", resolve);
+        stream.once("end", () => reject(new Error("read was not cancelled")));
+      });
+      stream.once("data", () => controller.abort());
+      const failure = await outcome;
+      expect(failure).toMatchObject({
+        name: "ArtifactReaderFailure",
+        reason: "cancelled",
+      });
+      await closed;
+      await new Promise<void>((resolve) => setImmediate(resolve));
+      await reader.close();
+    } finally {
+      await reader.close().catch(() => undefined);
+    }
+  });
+});
diff --git a/tests/boundary/filesystem/ownedArtifactReaderCleanup.test.ts b/tests/boundary/filesystem/ownedArtifactReaderCleanup.test.ts
new file mode 100644
index 0000000000..c9bc919ff9
--- /dev/null
+++ b/tests/boundary/filesystem/ownedArtifactReaderCleanup.test.ts
@@ -0,0 +1,140 @@
+import type { FileHandle } from "node:fs/promises";
+import { writeFile } from "node:fs/promises";
+import { join } from "node:path";
+
+import { expect, it, onTestFinished, vi } from "vitest";
+
+import { ArtifactResourceScope } from "../../../src/artifacts/ArtifactResourceScope.js";
+import { MachOSliceArtifactReader } from "../../../src/artifacts/MachOSliceArtifactReader.js";
+import { ZipArtifactReader } from "../../../src/artifacts/ZipArtifactReader.js";
+import { ok } from "../../../src/domain/result.js";
+import type { NativeCommandRunner } from "../../../src/native/CommandRunner.js";
+import { createTestTempDirectory } from "../../fixtures/temporaryDirectory.js";
+
+const injected = vi.hoisted(() => ({
+  opened: undefined as
+    | ((path: unknown, handle: FileHandle) => void)
+    | undefined,
+}));
+
+vi.mock("node:fs/promises", async (importOriginal) => {
+  const actual = await importOriginal<typeof import("node:fs/promises")>();
+  return {
+    ...actual,
+    open: async (...args: Parameters<typeof actual.open>) => {
+      const handle = await actual.open(...args);
+      injected.opened?.(args[0], handle);
+      return handle;
+    },
+  };
+});
+
+const runner: NativeCommandRunner = {
+  run: async () =>
+    ok({
+      tool: "lipo",
+      executable: "/usr/bin/lipo",
+      executableSha256: "1".repeat(64),
+      toolVersion: null,
+      versionReason: "fixture",
+      arguments: [],
+      stdout: "",
+      stderr: "",
+      stdoutBytes: 0,
+      stderrBytes: 0,
+      exitCode: 0,
+      signal: null,
+    }),
+};
+
+const readers = [
+  ["ZIP", (path: string) => new ZipArtifactReader(path, "zip")],
+  [
+    "Mach-O slice",
+    (path: string) => new MachOSliceArtifactReader(path, {}, runner),
+  ],
+] as const;
+
+it.each(readers)(
+  "retains %s reader admission and stat owners",
+  async (_, createReader) => {
+    const root = await createTestTempDirectory("rea-owned-reader-cleanup-");
+    const path = join(root, "source");
+    await writeFile(path, "fixture source");
+
+    for (const stage of ["admission", "post-open-stat"] as const) {
+      const statFailure = Object.assign(
+        new Error(`primary ${stage} stat failure`),
+        { code: "EIO", errno: -5, syscall: "fstat" },
+      );
+      const closeFailure = new Error(
+        `close failed after invalidation during ${stage}`,
+      );
+      let descriptor: FileHandle | undefined;
+      let statCalls = 0;
+      let closeAttempts = 0;
+      let failOnStat = stage === "admission" ? 1 : 2;
+      injected.opened = (openedPath, handle) => {
+        if (openedPath !== path || descriptor !== undefined) return;
+        descriptor = handle;
+        const stat = handle.stat.bind(handle);
+        const close = handle.close.bind(handle);
+        vi.spyOn(handle, "stat").mockImplementation(async (...args) => {
+          statCalls += 1;
+          if (statCalls === failOnStat) {
+            failOnStat = -1;
+            throw statFailure;
+          }
+          return stat(...args);
+        });
+        vi.spyOn(handle, "close").mockImplementation(async () => {
+          closeAttempts += 1;
+          await close();
+          throw closeFailure;
+        });
+      };
+
+      const reader = createReader(path);
+      const scope = new ArtifactResourceScope();
+      const owner = { kind: "reader" as const, resource: path, reader };
+      onTestFinished(async () => {
+        injected.opened = undefined;
+        await scope.close().catch(() => undefined);
+        vi.restoreAllMocks();
+      });
+
+      const primary = await (async () => {
+        try {
+          for await (const _entry of reader.entries()) {
+            // Both injected failures happen before the reader can yield an entry.
+          }
+        } catch (cause: unknown) {
+          return cause;
+        }
+        throw new Error("Expected reader initialization to fail");
+      })();
+      expect(primary).toBeInstanceOf(Error);
+      expect(causeChainContains(primary, statFailure)).toBe(true);
+
+      const release = await scope.release(owner);
+      expect(release).toEqual({ kind: "failed", cause: closeFailure });
+      expect(descriptor?.fd).toBe(-1);
+      await expect(scope.close()).rejects.toMatchObject({
+        reason: "unavailable",
+        cleanup: { reason: closeFailure.message, resources: [path] },
+      });
+      // Native close invalidated the fd before rejecting. Retrying the same owner
+      // must remain failed without another syscall or a false successful release.
+      expect(closeAttempts).toBe(1);
+    }
+  },
+);
+
+const causeChainContains = (cause: unknown, expected: unknown): boolean => {
+  let current: unknown = cause;
+  while (current instanceof Error) {
+    if (current === expected) return true;
+    current = current.cause;
+  }
+  return false;
+};
diff --git a/tests/fixtures/directoryReaderUnsupportedEntryProbe.mjs b/tests/fixtures/directoryReaderUnsupportedEntryProbe.mjs
new file mode 100644
index 0000000000..cc66c6e11d
--- /dev/null
+++ b/tests/fixtures/directoryReaderUnsupportedEntryProbe.mjs
@@ -0,0 +1,15 @@
+import { pathToFileURL } from "node:url";
+
+const [modulePath, root] = process.argv.slice(2);
+if (modulePath === undefined || root === undefined)
+  throw new Error("Directory reader probe requires module and root paths");
+
+const { DirectoryArtifactReader } = await import(pathToFileURL(modulePath));
+const reader = new DirectoryArtifactReader(root);
+const paths = [];
+try {
+  for await (const entry of reader.entries()) paths.push(entry.path);
+} finally {
+  await reader.close();
+}
+process.stdout.write(`${JSON.stringify(paths)}\n`);