diff --git a/docs/runtime/bunfig.md b/docs/runtime/bunfig.md
index 9ec995161d..ca0a36f7eb 100644
--- a/docs/runtime/bunfig.md
+++ b/docs/runtime/bunfig.md
@@ -651,7 +651,7 @@ editor = "code"
 
 The `bun run` command can be configured under the `[run]` section. These apply to the `bun run` command and the `bun` command when running a file or executable or script.
 
-Currently, `bunfig.toml` isn't always automatically loaded for `bun run` in a local project (it does check for a global `bunfig.toml`), so you might still need to pass `-c` or `-c=bunfig.toml` to use these settings.
+Currently, `bunfig.toml` is only automatically loaded for `bun run` in a local project (it doesn't check for a global `.bunfig.toml`).
 
 ### `run.shell` - use the system shell or Bun's shell
 
diff --git a/src/cli/run_command.zig b/src/cli/run_command.zig
index c72159c96c..34873d6819 100644
--- a/src/cli/run_command.zig
+++ b/src/cli/run_command.zig
@@ -1320,10 +1320,6 @@ pub const RunCommand = struct {
             };
         }
 
-        if (!ctx.debug.loaded_bunfig) {
-            bun.cli.Arguments.loadConfigPath(ctx.allocator, true, "bunfig.toml", ctx, .RunCommand) catch {};
-        }
-
         _ = _bootAndHandleError(ctx, absolute_script_path.?, null);
         return true;
     }
@@ -1368,11 +1364,14 @@ pub const RunCommand = struct {
             }
         }
 
+        if (!ctx.debug.loaded_bunfig) {
+            bun.cli.Arguments.loadConfigPath(ctx.allocator, true, "bunfig.toml", ctx, .RunCommand) catch {};
+        }
+
         // try fast run (check if the file exists and is not a folder, then run it)
         if (try_fast_run and maybeOpenWithBunJS(ctx)) return true;
 
         // setup
-
         const force_using_bun = ctx.debug.run_in_bun;
         var ORIGINAL_PATH: string = "";
         var this_transpiler: transpiler.Transpiler = undefined;
@@ -1380,10 +1379,6 @@ pub const RunCommand = struct {
         try configurePathForRun(ctx, root_dir_info, &this_transpiler, &ORIGINAL_PATH, root_dir_info.abs_path, force_using_bun);
         this_transpiler.env.map.put("npm_command", "run-script") catch unreachable;
 
-        if (!ctx.debug.loaded_bunfig) {
-            bun.cli.Arguments.loadConfigPath(ctx.allocator, true, "bunfig.toml", ctx, .RunCommand) catch {};
-        }
-
         // check for empty command
 
         if (target_name.len == 0) {
diff --git a/test/cli/install/bun-run-bunfig.test.ts b/test/cli/install/bun-run-bunfig.test.ts
index a5890fb92d..c3a90d514c 100644
--- a/test/cli/install/bun-run-bunfig.test.ts
+++ b/test/cli/install/bun-run-bunfig.test.ts
@@ -1,6 +1,7 @@
 import { describe, expect, test } from "bun:test";
 import { realpathSync } from "fs";
 import { bunEnv, bunExe, isWindows, tempDirWithFiles, toTOMLString } from "harness";
+import { join as pathJoin } from "node:path";
 
 describe.each(["bun run", "bun"])(`%s`, cmd => {
   const runCmd = cmd === "bun" ? ["-c=bunfig.toml", "run"] : ["-c=bunfig.toml"];
@@ -131,4 +132,119 @@ describe.each(["bun run", "bun"])(`%s`, cmd => {
       expect(result.success).toBeFalse();
     });
   });
+
+  test("autoload local bunfig.toml (same cwd)", async () => {
+    const runCmd = cmd === "bun" ? ["run"] : [];
+
+    const bunfig = toTOMLString({
+      run: {
+        bun: true,
+      },
+    });
+
+    const cwd = tempDirWithFiles("run.where.node", {
+      "bunfig.toml": bunfig,
+      "package.json": JSON.stringify(
+        {
+          scripts: {
+            "where-node": `which node`,
+          },
+        },
+        null,
+        2,
+      ),
+    });
+
+    const result = Bun.spawnSync({
+      cmd: [bunExe(), "--silent", ...runCmd, "where-node"],
+      env: bunEnv,
+      stderr: "inherit",
+      stdout: "pipe",
+      stdin: "ignore",
+      cwd,
+    });
+    const nodeBin = result.stdout.toString().trim();
+
+    if (isWindows) {
+      expect(realpathSync(nodeBin)).toContain("\\bun-node-");
+    } else {
+      expect(realpathSync(nodeBin)).toBe(realpathSync(execPath));
+    }
+  });
+
+  test("NOT autoload local bunfig.toml (sub cwd)", async () => {
+    const runCmd = cmd === "bun" ? ["run"] : [];
+
+    const bunfig = toTOMLString({
+      run: {
+        bun: true,
+      },
+    });
+
+    const cwd = tempDirWithFiles("run.where.node", {
+      "bunfig.toml": bunfig,
+      "package.json": JSON.stringify(
+        {
+          scripts: {
+            "where-node": `which node`,
+          },
+        },
+        null,
+        2,
+      ),
+      "subdir/a.txt": "a",
+    });
+
+    const result = Bun.spawnSync({
+      cmd: [bunExe(), "--silent", ...runCmd, "where-node"],
+      env: bunEnv,
+      stderr: "inherit",
+      stdout: "pipe",
+      stdin: "ignore",
+      cwd: pathJoin(cwd, "./subdir"),
+    });
+    const nodeBin = result.stdout.toString().trim();
+
+    expect(realpathSync(nodeBin)).toBe(realpathSync(node));
+    expect(result.success).toBeTrue();
+  });
+
+  test("NOT autoload home bunfig.toml", async () => {
+    const runCmd = cmd === "bun" ? ["run"] : [];
+
+    const bunfig = toTOMLString({
+      run: {
+        bun: true,
+      },
+    });
+
+    const cwd = tempDirWithFiles("run.where.node", {
+      "my-home/.bunfig.toml": bunfig,
+      "package.json": JSON.stringify(
+        {
+          scripts: {
+            "where-node": `which node`,
+          },
+        },
+        null,
+        2,
+      ),
+    });
+
+    const result = Bun.spawnSync({
+      cmd: [bunExe(), "--silent", ...runCmd, "where-node"],
+      env: {
+        ...bunEnv,
+        HOME: pathJoin(cwd, "./my-home"),
+      },
+      stderr: "inherit",
+      stdout: "pipe",
+      stdin: "ignore",
+      cwd,
+    });
+    const nodeBin = result.stdout.toString().trim();
+
+    expect(realpathSync(nodeBin)).toBe(realpathSync(node));
+    expect(result.success).toBeTrue();
+  });
 });