diff --git a/src/spawn_sys/spawn_process.rs b/src/spawn_sys/spawn_process.rs
index 2ec26ae2edd2..3684795f6e2a 100644
--- a/src/spawn_sys/spawn_process.rs
+++ b/src/spawn_sys/spawn_process.rs
@@ -596,6 +596,19 @@ struct PosixSpawnFdGuard {
     on_error: bool,
 }
 
+#[cfg(unix)]
+impl PosixSpawnFdGuard {
+    /// File actions run in slot order, so an earlier slot's `close`/`dup2` would hit a `dup2` source numbered at or below `max_slot`; dup it above every slot first, like libuv.
+    fn source_above_slots(&mut self, max_slot: i32, src: Fd) -> bun_sys::Result<Fd> {
+        if src.native() > max_slot {
+            return Ok(src);
+        }
+        let moved = bun_sys::dup_at_least(src, max_slot + 1)?;
+        self.to_close_at_end.push(moved);
+        Ok(moved)
+    }
+}
+
 #[cfg(unix)]
 impl Drop for PosixSpawnFdGuard {
     fn drop(&mut self) {
@@ -716,12 +729,37 @@ pub unsafe fn spawn_process_posix(
     let _ = attr.set(flags as _);
     let _ = attr.reset_signals();
 
+    // Highest child fd that a file action targets: stderr, or the last extra slot.
+    let Ok(max_slot) = FdT::try_from(2 + options.extra_fds.len()) else {
+        return Ok(Err(bun_sys::Error::from_code(
+            bun_sys::E::EMFILE,
+            bun_sys::Tag::posix_spawn,
+        )));
+    };
+
     if let Some(ipc) = options.ipc {
         actions.inherit(ipc)?;
         spawned.ipc = Some(ipc);
     }
 
     let stdio_options: [&PosixStdio; 3] = [&options.stdin, &options.stdout, &options.stderr];
+    // Probed before this function creates any fd: a socketpair end can land on a closed slot number and make that slot look open.
+    let inherits_closed_fd = |stdio: &PosixStdio, slot: usize| {
+        matches!(stdio, PosixStdio::Inherit)
+            && bun_sys::get_fcntl_flags(Fd::from_native(slot as FdT)).is_err()
+    };
+    let closed_stdio: [bool; 3] = core::array::from_fn(|i| inherits_closed_fd(stdio_options[i], i));
+    if options
+        .extra_fds
+        .iter()
+        .enumerate()
+        .any(|(i, stdio)| inherits_closed_fd(stdio, 3 + i))
+    {
+        return Ok(Err(bun_sys::Error::from_code(
+            bun_sys::E::EBADF,
+            bun_sys::Tag::posix_spawn,
+        )));
+    }
     // Reshaped for borrowck: we
     // index spawned.{stdin,stdout,stderr} via a helper closure.
     let mut dup_stdout_to_stderr: bool = false;
@@ -756,9 +794,11 @@ pub unsafe fn spawn_process_posix(
             }
             PosixStdio::Inherit => {
                 // A closed slot would inherit whatever fd is created later at that number (e.g. the ipc socketpair); libuv gives it /dev/null.
-                if bun_sys::get_fcntl_flags(fileno).is_err() {
+                if closed_stdio[i] {
                     actions.open_z(fileno, c"/dev/null", flag | bun_sys::O::CREAT as u32, 0o664)?;
                 } else {
+                    // O_NONBLOCK is on the shared open file description: left set (by `process.stdout` on a pipe), the child's plain write(2) fails with EAGAIN. libuv clears it too.
+                    let _ = bun_sys::update_nonblocking(fileno, false);
                     actions.inherit(fileno)?;
                 }
             }
@@ -788,7 +828,11 @@ pub unsafe fn spawn_process_posix(
 
                         cleanup.to_close_on_error.push(fd);
                         cleanup.to_set_cloexec.push(fd);
-                        actions.dup2(fd, fileno)?;
+                        let src = match cleanup.source_above_slots(max_slot, fd) {
+                            Ok(src) => src,
+                            Err(e) => return Ok(Err(e)),
+                        };
+                        actions.dup2(src, fileno)?;
                         set_spawned_stdio(&mut spawned, i, fd);
                         spawned.memfds[i] = true;
                         continue 'stdio;
@@ -869,15 +913,24 @@ pub unsafe fn spawn_process_posix(
                     }
                 }
 
-                actions.dup2(fds[1], fileno)?;
-                if fds[1] != fileno {
+                let src = match cleanup.source_above_slots(max_slot, fds[1]) {
+                    Ok(src) => src,
+                    Err(e) => return Ok(Err(e)),
+                };
+                actions.dup2(src, fileno)?;
+                if src == fds[1] {
                     actions.close(fds[1])?;
                 }
 
                 set_spawned_stdio(&mut spawned, i, fds[0]);
             }
             PosixStdio::Pipe(fd) => {
-                actions.dup2(*fd, fileno)?;
+                let _ = bun_sys::update_nonblocking(*fd, false);
+                let src = match cleanup.source_above_slots(max_slot, *fd) {
+                    Ok(src) => src,
+                    Err(e) => return Ok(Err(e)),
+                };
+                actions.dup2(src, fileno)?;
                 set_spawned_stdio(&mut spawned, i, *fd);
             }
             PosixStdio::SocketFd => {
@@ -919,24 +972,28 @@ pub unsafe fn spawn_process_posix(
                 extra_fds.push(ExtraPipe::Unavailable);
             }
             PosixStdio::Ipc | PosixStdio::Buffer | PosixStdio::SocketFd => {
-                let is_ipc = matches!(ipc, PosixStdio::Ipc);
+                // Only the parent's end goes nonblocking: a child that is not bun or node does a plain write(2) on its end, and libuv hands out a blocking one too.
                 let fds: [Fd; 2] =
-                    match bun_sys::socketpair(libc::AF_UNIX, libc::SOCK_STREAM, 0, is_ipc) {
+                    match bun_sys::socketpair(libc::AF_UNIX, libc::SOCK_STREAM, 0, false) {
                         Ok(p) => p,
                         Err(e) => return Ok(Err(e)),
                     };
 
-                if !options.sync && !is_ipc {
+                cleanup.to_close_at_end.push(fds[1]);
+                cleanup.to_close_on_error.push(fds[0]);
+
+                if !options.sync {
                     if let Err(e) = bun_sys::set_nonblocking(fds[0]) {
                         return Ok(Err(e));
                     }
                 }
 
-                cleanup.to_close_at_end.push(fds[1]);
-                cleanup.to_close_on_error.push(fds[0]);
-
-                actions.dup2(fds[1], fileno)?;
-                if fds[1] != fileno {
+                let src = match cleanup.source_above_slots(max_slot, fds[1]) {
+                    Ok(src) => src,
+                    Err(e) => return Ok(Err(e)),
+                };
+                actions.dup2(src, fileno)?;
+                if src == fds[1] {
                     actions.close(fds[1])?;
                 }
                 // SocketFd: push as OwnedFd here so every error path between
@@ -949,7 +1006,11 @@ pub unsafe fn spawn_process_posix(
                 extra_fds.push(ExtraPipe::OwnedFd(fds[0]));
             }
             PosixStdio::Pipe(fd) => {
-                actions.dup2(*fd, fileno)?;
+                let src = match cleanup.source_above_slots(max_slot, *fd) {
+                    Ok(src) => src,
+                    Err(e) => return Ok(Err(e)),
+                };
+                actions.dup2(src, fileno)?;
                 // The fd was supplied by the caller (a number in the stdio array) and is
                 // not owned by us. Record it so `stdio[N]` returns the caller's fd, but
                 // mark it unowned so finalizeStreams leaves it open.
diff --git a/test/js/bun/spawn/fixtures/fd-nonblock-probe.js b/test/js/bun/spawn/fixtures/fd-nonblock-probe.js
new file mode 100644
index 000000000000..e0b505f3c68b
--- /dev/null
+++ b/test/js/bun/spawn/fixtures/fd-nonblock-probe.js
@@ -0,0 +1,28 @@
+// Prints "<fd>:blocking" or "<fd>:nonblocking" for each fd number in argv.
+// The flag is read before anything writes, so this process cannot change it.
+// Must not touch process.stdout/process.stderr/process.send: those set
+// O_NONBLOCK on their own fds.
+import { dlopen } from "bun:ffi";
+import { existsSync, readFileSync } from "node:fs";
+
+let isNonblocking;
+if (existsSync("/proc/self/fdinfo")) {
+  isNonblocking = fd => {
+    const flags = readFileSync(`/proc/self/fdinfo/${fd}`, "utf8").match(/^flags:\s*([0-7]+)/m)[1];
+    return (parseInt(flags, 8) & 0o4000) !== 0;
+  };
+} else {
+  // F_GETFL is 3 on every platform here. O_NONBLOCK is 0o4000 on Linux and 4 on macOS and the BSDs.
+  const libc = { darwin: "libSystem.B.dylib", freebsd: "libc.so.7" }[process.platform] ?? "libc.so.6";
+  const O_NONBLOCK = process.platform === "linux" ? 0o4000 : 4;
+  const { fcntl } = dlopen(libc, {
+    fcntl: { args: ["i32", "i32", "i32"], returns: "i32" },
+  }).symbols;
+  isNonblocking = fd => (fcntl(fd, 3, 0) & O_NONBLOCK) !== 0;
+}
+
+const out = process.argv
+  .slice(2)
+  .map(arg => `${arg}:${isNonblocking(Number(arg)) ? "nonblocking" : "blocking"}`)
+  .join(" ");
+console.log(out);
diff --git a/test/js/bun/spawn/spawn.test.ts b/test/js/bun/spawn/spawn.test.ts
index a9003d595c48..6ceb17bd36c2 100644
--- a/test/js/bun/spawn/spawn.test.ts
+++ b/test/js/bun/spawn/spawn.test.ts
@@ -1841,3 +1841,206 @@ it.if(parentThp() === "1")("spawned children keep the system THP policy", async
   expect(thpEnabled(readFileSync("/proc/self/status", "utf8"))).toBe("1");
   expect(exitCode).toBe(0);
 });
+
+// Runs a script in a fresh bun process, so its fd numbers are low and known and a blocked spawnSync cannot block this runner.
+async function runInFreshProcess(script: string) {
+  await using proc = spawn({
+    cmd: [bunExe(), "-e", script],
+    env: bunEnv,
+    stdio: ["ignore", "pipe", "pipe"],
+  });
+  const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+  return { stdout, stderr, exitCode };
+}
+
+// O_NONBLOCK lives on the open file description, so a flag bun sets on its
+// own stdout or on a socketpair end reaches any child that shares it. A child
+// that is not bun or node then fails a plain write(2) with EAGAIN.
+describe.skipIf(!isPosix)("file status flags handed to the child", () => {
+  const probe = join(import.meta.dir, "fixtures", "fd-nonblock-probe.js");
+
+  it.concurrent("stdout and stderr inherited after the parent used process.stdout/stderr are blocking", async () => {
+    await using proc = spawn({
+      cmd: [
+        bunExe(),
+        "-e",
+        `process.stdout.write("out\\n");
+         process.stderr.write("err\\n");
+         const r = Bun.spawnSync([process.execPath, ${JSON.stringify(probe)}, "1", "2"], { stdout: "inherit", stderr: "inherit" });
+         process.exit(r.exitCode);`,
+      ],
+      env: bunEnv,
+      stdout: "pipe",
+      stderr: "pipe",
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+    expect(stdout).toBe("out\n1:blocking 2:blocking\n");
+    expect(stderr).toBe("err\n");
+    expect(exitCode).toBe(0);
+  });
+
+  it.concurrent("the ipc fd is blocking", async () => {
+    await using proc = spawn({
+      cmd: [bunExe(), probe, "3"],
+      env: bunEnv,
+      stdout: "pipe",
+      stderr: "pipe",
+      ipc() {},
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+    expect(stdout).toBe("3:blocking\n");
+    expect(stderr).toBe("");
+    expect(exitCode).toBe(0);
+  });
+
+  it.concurrent("a plain tool writing more than the pipe holds succeeds on inherited stdout", async () => {
+    // The user-visible shape of the test above: with fd 1 nonblocking, head
+    // gets EAGAIN as soon as it outruns this reader and exits 1 with a short
+    // count. (If the reader keeps up, head never sees a full pipe, so the
+    // flag probe above is the deterministic check.)
+    await using proc = spawn({
+      cmd: [
+        bunExe(),
+        "-e",
+        `process.stdout.write("start\\n");
+         const r = Bun.spawnSync(["head", "-c", "1000000", "/dev/zero"], { stdout: "inherit", stderr: "inherit" });
+         process.stderr.write("rc=" + r.exitCode + "\\n");`,
+      ],
+      env: bunEnv,
+      stdout: "pipe",
+      stderr: "pipe",
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.bytes(), proc.stderr.text(), proc.exited]);
+    expect(stderr).toBe("rc=0\n");
+    expect(stdout.byteLength).toBe("start\n".length + 1000000);
+    expect(exitCode).toBe(0);
+  });
+});
+
+describe.skipIf(!isPosix)("stdio source fds that are also slot numbers", () => {
+  // File actions run in slot order in the child. The source fd of a later
+  // slot must survive the actions of the slots before it (the close of an
+  // "ignore" slot, the dup2 onto another slot) even when its fd number is one
+  // of those slots. Each case runs in a fresh process so the source fds are
+  // low, known numbers.
+  it.concurrent("a pipe after many ignore slots", async () => {
+    const slots = 60;
+    const result = await runInFreshProcess(`
+      const fs = require("fs");
+      const proc = Bun.spawn({
+        cmd: [process.execPath, "-e", "require('fs').writeSync(${slots}, 'hi')"],
+        stdio: ["ignore", "inherit", "inherit", ...Array(${slots - 3}).fill("ignore"), "pipe"],
+      });
+      const fd = proc.stdio[${slots}];
+      const exitCode = await proc.exited;
+      const buf = Buffer.alloc(16);
+      const n = fs.readSync(fd, buf);
+      console.log(JSON.stringify({ sourceBelowSlot: fd < ${slots}, exitCode, data: buf.toString("utf8", 0, n) }));
+    `);
+    expect(result.stderr).toBe("");
+    expect(JSON.parse(result.stdout)).toEqual({ sourceBelowSlot: true, exitCode: 0, data: "hi" });
+    expect(result.exitCode).toBe(0);
+  });
+
+  it.concurrent("a caller fd after many ignore slots", async () => {
+    using dir = tempDir("spawn-high-slot", {});
+    const slots = 60;
+    const file = join(String(dir), "out.txt");
+    const result = await runInFreshProcess(`
+      const fs = require("fs");
+      const fd = fs.openSync(${JSON.stringify(file)}, "w");
+      const proc = Bun.spawn({
+        cmd: [process.execPath, "-e", "require('fs').writeSync(${slots}, 'hi')"],
+        stdio: ["ignore", "inherit", "inherit", ...Array(${slots - 3}).fill("ignore"), fd],
+      });
+      console.log(JSON.stringify({ sourceBelowSlot: fd < ${slots}, exitCode: await proc.exited }));
+    `);
+    expect(result.stderr).toBe("");
+    expect(JSON.parse(result.stdout)).toEqual({ sourceBelowSlot: true, exitCode: 0 });
+    expect(readFileSync(file, "utf8")).toBe("hi");
+    expect(result.exitCode).toBe(0);
+  });
+
+  it.concurrent("fd 2 at stdout and fd 1 at stderr swap them", async () => {
+    const result = await runInFreshProcess(`
+      const proc = Bun.spawn({
+        cmd: [process.execPath, "-e", "require('fs').writeSync(1, 'to-fd-1,'); require('fs').writeSync(2, 'to-fd-2,')"],
+        stdio: ["ignore", 2, 1],
+      });
+      await proc.exited;
+    `);
+    expect({ stdout: result.stdout, stderr: result.stderr }).toEqual({ stdout: "to-fd-2,", stderr: "to-fd-1," });
+    expect(result.exitCode).toBe(0);
+  });
+
+  // The child reports which of its fds 1 and 2 is /dev/null. It writes the report to the other one.
+  const reportDevNull = (reportFd: 1 | 2) => `
+    const fs = require("fs");
+    const devNull = fs.statSync("/dev/null").rdev;
+    const isDevNull = fd => { const s = fs.fstatSync(fd); return s.isCharacterDevice() && s.rdev === devNull; };
+    fs.writeSync(${reportFd}, JSON.stringify({ stdoutIsDevNull: isDevNull(1), stderrIsDevNull: isDevNull(2) }));
+  `;
+
+  it.concurrent(
+    "a closed stdout slot that is inherited gets /dev/null, not the stdin pipe end that took fd 1",
+    async () => {
+      const result = await runInFreshProcess(`
+      require("fs").closeSync(1);
+      // stdin "pipe" makes a socketpair, and its child end lands on the free fd 1.
+      const proc = Bun.spawn({
+        cmd: [process.execPath, "-e", ${JSON.stringify(reportDevNull(2))}],
+        stdio: ["pipe", "inherit", "inherit"],
+      });
+      process.exitCode = await proc.exited;
+    `);
+      expect(JSON.parse(result.stderr)).toEqual({ stdoutIsDevNull: true, stderrIsDevNull: false });
+      expect(result.exitCode).toBe(0);
+    },
+  );
+
+  it.concurrent(
+    "a closed stderr slot that is inherited gets /dev/null, not the stdout pipe end that took fd 2",
+    async () => {
+      const result = await runInFreshProcess(`
+      require("fs").closeSync(2);
+      // stdout "pipe" makes a socketpair, and the parent's end lands on the free fd 2.
+      const proc = Bun.spawn({
+        cmd: [process.execPath, "-e", ${JSON.stringify(reportDevNull(1))}],
+        stdio: ["ignore", "pipe", "inherit"],
+      });
+      const [report, exitCode] = await Promise.all([proc.stdout.text(), proc.exited]);
+      console.log(report);
+      process.exitCode = exitCode;
+    `);
+      expect(JSON.parse(result.stdout)).toEqual({ stdoutIsDevNull: false, stderrIsDevNull: true });
+      expect(result.exitCode).toBe(0);
+    },
+  );
+
+  it.concurrent(
+    "an extra inherit slot that is closed in the parent fails with EBADF, not with the pipe end that took its number",
+    async () => {
+      const result = await runInFreshProcess(`
+      const fs = require("fs");
+      const free = fs.openSync("/dev/null", "r"); // the lowest free fd number
+      fs.closeSync(free);
+      let outcome;
+      try {
+        // stdin "pipe" makes a socketpair, and its child end lands on that free number.
+        const proc = Bun.spawn({
+          cmd: ["true"],
+          stdio: ["pipe", "inherit", "inherit", ...Array(free - 3).fill("ignore"), "inherit"],
+        });
+        await proc.exited;
+        outcome = "spawned";
+      } catch (e) {
+        outcome = e.code;
+      }
+      console.log(JSON.stringify({ freeIsExtraSlot: free >= 3, outcome }));
+    `);
+      expect(result.stderr).toBe("");
+      expect(JSON.parse(result.stdout)).toEqual({ freeIsExtraSlot: true, outcome: "EBADF" });
+      expect(result.exitCode).toBe(0);
+    },
+  );
+});
diff --git a/test/js/node/child_process/child-process-stdio.test.js b/test/js/node/child_process/child-process-stdio.test.js
index 78b6454f9243..ae6a3d4a3ba4 100644
--- a/test/js/node/child_process/child-process-stdio.test.js
+++ b/test/js/node/child_process/child-process-stdio.test.js
@@ -1,7 +1,8 @@
 import { describe, expect, it } from "bun:test";
-import { bunEnv, bunExe } from "harness";
+import { bunEnv, bunExe, isPosix } from "harness";
 import { execSync, spawn } from "node:child_process";
 import { once } from "node:events";
+import { join } from "node:path";
 
 const CHILD_PROCESS_FILE = import.meta.dir + "/spawned-child.js";
 const OUT_FILE = import.meta.dir + "/stdio-test-out.txt";
@@ -166,3 +167,81 @@ describe("child.stdin", () => {
     });
   });
 });
+
+describe.skipIf(!isPosix)("stdio handed to the child", () => {
+  // Prints whether O_NONBLOCK is set on each fd number given in argv.
+  const probe = join(import.meta.dir, "..", "..", "bun", "spawn", "fixtures", "fd-nonblock-probe.js");
+
+  it.concurrent("inherited stdio is blocking after the parent used process.stdout", async () => {
+    // The parent's fd 1 and 2 are pipes here. process.stdout.write() sets
+    // O_NONBLOCK on the shared open file description; a child that is not
+    // bun or node then fails a plain write(2) with EAGAIN once the pipe fills.
+    await using proc = Bun.spawn({
+      cmd: [
+        bunExe(),
+        "-e",
+        `const { spawnSync } = require("node:child_process");
+         process.stdout.write("out\\n");
+         process.stderr.write("err\\n");
+         const sync = spawnSync(process.execPath, [${JSON.stringify(probe)}, "0", "1", "2"], { stdio: "inherit" });
+         process.exit(sync.status ?? 1);`,
+      ],
+      env: bunEnv,
+      stdin: "pipe",
+      stdout: "pipe",
+      stderr: "pipe",
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+    expect(stderr).toBe("err\n");
+    expect(stdout).toBe("out\n0:blocking 1:blocking 2:blocking\n");
+    expect(exitCode).toBe(0);
+  });
+
+  it.concurrent("the ipc fd is blocking", async () => {
+    // A child that is not bun or node does a plain write(2) on NODE_CHANNEL_FD.
+    // On an O_NONBLOCK socket a large message is cut short and lost.
+    await using proc = Bun.spawn({
+      cmd: [
+        bunExe(),
+        "-e",
+        `const { spawn } = require("node:child_process");
+         const child = spawn(process.execPath, [${JSON.stringify(probe)}, "3"], { stdio: ["inherit", "inherit", "inherit", "ipc"] });
+         child.on("exit", code => process.exit(code ?? 1));`,
+      ],
+      env: bunEnv,
+      stdout: "pipe",
+      stderr: "pipe",
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+    expect(stderr).toBe("");
+    expect(stdout).toBe("3:blocking\n");
+    expect(exitCode).toBe(0);
+  });
+
+  it.concurrent("a pipe slot after many ignore slots", async () => {
+    // Run in a fresh process so the pipe's source fd is a low number, below
+    // the slot it is dup2'd to. The close of each "ignore" slot used to hit it,
+    // and spawn() then threw EBADF synchronously.
+    const slots = 60;
+    await using proc = Bun.spawn({
+      cmd: [
+        bunExe(),
+        "-e",
+        `const { spawn, spawnSync } = require("node:child_process");
+         const stdio = ["ignore", "ignore", "ignore", ...Array(${slots - 3}).fill("ignore"), "pipe"];
+         const sync = spawnSync("true", [], { stdio });
+         console.log("spawnSync:", sync.error?.code ?? "ok", sync.status);
+         const child = spawn("true", [], { stdio });
+         child.on("error", e => console.log("error event", e.code));
+         child.on("exit", code => console.log("spawn:", code));`,
+      ],
+      env: bunEnv,
+      stdout: "pipe",
+      stderr: "pipe",
+    });
+    const [stdout, stderr, exitCode] = await Promise.all([proc.stdout.text(), proc.stderr.text(), proc.exited]);
+    expect(stderr).toBe("");
+    expect(stdout).toBe("spawnSync: ok 0\nspawn: 0\n");
+    expect(exitCode).toBe(0);
+  });
+});