diff --git a/src/bun.js/webcore/blob/read_file.zig b/src/bun.js/webcore/blob/read_file.zig
index db36497de4a..05c07df4885 100644
--- a/src/bun.js/webcore/blob/read_file.zig
+++ b/src/bun.js/webcore/blob/read_file.zig
@@ -384,8 +384,9 @@ pub const ReadFile = struct {
 
         // add an extra 16 bytes to the buffer to avoid having to resize it for trailing extra data
         if (!this.could_block or (this.size > 0 and this.size != Blob.max_size))
-            this.buffer = std.ArrayListUnmanaged(u8).initCapacity(bun.default_allocator, this.size + 16) catch |err| {
+            this.buffer = std.ArrayListUnmanaged(u8).initCapacity(bun.default_allocator, this.size +| 16) catch |err| {
                 this.errno = err;
+                this.system_error = bun.sys.Error.fromCode(bun.sys.E.NOMEM, .read).toSystemError();
                 this.onFinish();
                 return;
             };
diff --git a/test/js/bun/util/bun-file-read.test.ts b/test/js/bun/util/bun-file-read.test.ts
index fd8bca82ac3..e3a4cc7747f 100644
--- a/test/js/bun/util/bun-file-read.test.ts
+++ b/test/js/bun/util/bun-file-read.test.ts
@@ -1,4 +1,5 @@
 import { expect, it } from "bun:test";
+import { isPosix } from "harness";
 import { tmpdir } from "node:os";
 
 it("offset should work in Bun.file() #4963", async () => {
@@ -9,3 +10,13 @@ it("offset should work in Bun.file() #4963", async () => {
   const contents = await slice.text();
   expect(contents).toBe("ntents");
 });
+
+it.skipIf(!isPosix)("slicing Bun.file() by a non-zero offset rejects rather than overflowing", async () => {
+  // Regression: ReadFile.runAsyncWithFD computed buffer capacity as
+  // `this.size + 16`, which overflowed u52 when `this.size` approached
+  // Blob.max_size (2^52 - 1). The fix uses saturating addition and
+  // propagates the OOM via system_error so the promise rejects with ENOMEM.
+  const file = Bun.file("/dev/zero");
+  const sliced = file.slice(1);
+  await expect(sliced.text()).rejects.toMatchObject({ code: "ENOMEM" });
+});