diff --git a/testing/file_test/autoupdate.cpp b/testing/file_test/autoupdate.cpp
index 718d7e60f8d3..b945e42feea6 100644
--- a/testing/file_test/autoupdate.cpp
+++ b/testing/file_test/autoupdate.cpp
@@ -286,17 +286,18 @@ auto AutoupdateFileTest(
               .insert({non_check_line.line_number(), ++output_line_number})
               .second);
 
+      // If we just added the AUTOUPDATE line, include any early STDERR lines
+      // now, so that the initial batch of CHECK lines have STDERR before
+      // STDOUT. This also ensures we don't insert a blank line before the
+      // STDERR checks if there are no more lines after AUTOUPDATE.
+      if (autoupdate_line_number == non_check_line.line_number()) {
+        add_check_lines(stderr_check_lines, stderr_check_line,
+                        non_check_line.line_number(), non_check_line.indent());
+      }
+
       // STDOUT check lines are placed after the line they refer to, or at the
       // end of the file if none of them refers to a line.
       if (reached_autoupdate && any_attached_stdout_lines) {
-        // Include any early STDERR lines now, so that the initial batch of
-        // CHECK lines have STDERR before STDOUT.
-        if (autoupdate_line_number == non_check_line.line_number()) {
-          add_check_lines(stderr_check_lines, stderr_check_line,
-                          non_check_line.line_number(),
-                          non_check_line.indent());
-        }
-
         add_check_lines(stdout_check_lines, stdout_check_line,
                         non_check_line.line_number(), non_check_line.indent());
       }
diff --git a/toolchain/driver/testdata/fail_missing_file.carbon b/toolchain/driver/testdata/fail_missing_file.carbon
index 45528c34d07c..3d87be4cd51d 100644
--- a/toolchain/driver/testdata/fail_missing_file.carbon
+++ b/toolchain/driver/testdata/fail_missing_file.carbon
@@ -5,5 +5,4 @@
 // ARGS: compile --phase=lex nonexistent.carbon
 //
 // AUTOUPDATE
-
 // CHECK:STDERR: nonexistent.carbon: Error opening file for read: No such file or directory