diff --git a/testing/file_test/autoupdate.cpp b/testing/file_test/autoupdate.cpp
index 8a4b9ba9e4fb..71ef731f268e 100644
--- a/testing/file_test/autoupdate.cpp
+++ b/testing/file_test/autoupdate.cpp
@@ -225,11 +225,13 @@ auto FileTestAutoupdater::AddCheckLines(CheckLines& check_lines,
   }
 }
 
-auto FileTestAutoupdater::FinishFile() -> void {
+auto FileTestAutoupdater::FinishFile(bool is_last_file) -> void {
+  bool include_stdout = any_attached_stdout_lines_ || is_last_file;
+
   // At the end of each file, print any remaining lines which are associated
   // with the file.
   if (ShouldAddCheckLine(stderr_, INT_MAX) ||
-      ShouldAddCheckLine(stdout_, INT_MAX)) {
+      (include_stdout && ShouldAddCheckLine(stdout_, INT_MAX))) {
     // Ensure there's a blank line before any trailing CHECKs.
     if (!new_lines_.empty() && !new_lines_.back()->is_blank()) {
       new_lines_.push_back(&blank_line_);
@@ -237,7 +239,9 @@ auto FileTestAutoupdater::FinishFile() -> void {
     }
 
     AddCheckLines(stderr_, INT_MAX, "");
-    AddCheckLines(stdout_, INT_MAX, "");
+    if (include_stdout) {
+      AddCheckLines(stdout_, INT_MAX, "");
+    }
   }
 
   new_last_line_numbers_.push_back(output_line_number_);
@@ -292,7 +296,7 @@ auto FileTestAutoupdater::Run(bool dry_run) -> bool {
   // Loop through remaining content.
   while (non_check_line_ != non_check_lines_.end()) {
     if (output_file_number_ < non_check_line_->file_number()) {
-      FinishFile();
+      FinishFile(/*is_last_file=*/false);
       StartSplitFile();
       continue;
     }
@@ -314,7 +318,7 @@ auto FileTestAutoupdater::Run(bool dry_run) -> bool {
     ++non_check_line_;
   }
 
-  FinishFile();
+  FinishFile(/*is_last_file=*/true);
 
   for (auto& check_line : stdout_.lines) {
     check_line.RemapLineNumbers(output_line_remap_, new_last_line_numbers_);
diff --git a/testing/file_test/autoupdate.h b/testing/file_test/autoupdate.h
index 57d41ac557ad..169698fc59c5 100644
--- a/testing/file_test/autoupdate.h
+++ b/testing/file_test/autoupdate.h
@@ -160,8 +160,10 @@ class FileTestAutoupdater {
   auto AddCheckLines(CheckLines& check_lines, int to_line_number,
                      llvm::StringRef indent) -> void;
 
-  // Adds remaining check lines for the current file.
-  auto FinishFile() -> void;
+  // Adds remaining check lines for the current file. stderr is always included,
+  // but stdout is only included when either any_attached_stdout_lines_ or
+  // is_last_file is true.
+  auto FinishFile(bool is_last_file) -> void;
 
   // Starts a new split file, updating file and line numbers. Advances past the
   // split line.
diff --git a/testing/file_test/testdata/unattached_multi_file.carbon b/testing/file_test/testdata/unattached_multi_file.carbon
index 3366a997a623..7c54423489e3 100644
--- a/testing/file_test/testdata/unattached_multi_file.carbon
+++ b/testing/file_test/testdata/unattached_multi_file.carbon
@@ -6,11 +6,12 @@
 // CHECK:STDERR: unattached message 3
 // CHECK:STDERR: unattached message 4
 
-// CHECK:STDOUT: 3 args: `default_args`, `a.carbon`, `b.carbon`
-// CHECK:STDOUT: unattached message 1
-// CHECK:STDOUT: unattached message 2
 // --- a.carbon
 aaa
 
 // --- b.carbon
 bbb
+
+// CHECK:STDOUT: 3 args: `default_args`, `a.carbon`, `b.carbon`
+// CHECK:STDOUT: unattached message 1
+// CHECK:STDOUT: unattached message 2
diff --git a/toolchain/check/testdata/basics/multifile.carbon b/toolchain/check/testdata/basics/multifile.carbon
index c2c30c0416b8..3347f8c10108 100644
--- a/toolchain/check/testdata/basics/multifile.carbon
+++ b/toolchain/check/testdata/basics/multifile.carbon
@@ -4,6 +4,12 @@
 //
 // AUTOUPDATE
 
+// --- a.carbon
+fn A() {}
+
+// --- b.carbon
+fn B() {}
+
 // CHECK:STDOUT: file "a.carbon" {
 // CHECK:STDOUT:   %.loc1 = fn_decl @A
 // CHECK:STDOUT: }
@@ -20,8 +26,3 @@
 // CHECK:STDOUT: !entry:
 // CHECK:STDOUT:   return
 // CHECK:STDOUT: }
-// --- a.carbon
-fn A() {}
-
-// --- b.carbon
-fn B() {}
diff --git a/toolchain/check/testdata/basics/multifile_raw_and_textual_ir.carbon b/toolchain/check/testdata/basics/multifile_raw_and_textual_ir.carbon
index 0f3faa5abebd..5bda8f220213 100644
--- a/toolchain/check/testdata/basics/multifile_raw_and_textual_ir.carbon
+++ b/toolchain/check/testdata/basics/multifile_raw_and_textual_ir.carbon
@@ -8,6 +8,12 @@
 //
 // AUTOUPDATE
 
+// --- a.carbon
+fn A() {}
+
+// --- b.carbon
+fn B() {}
+
 // CHECK:STDOUT: - filename: a.carbon
 // CHECK:STDOUT:   sem_ir:
 // CHECK:STDOUT:   - cross_reference_irs_size: 1
@@ -88,8 +94,3 @@
 // CHECK:STDOUT: !entry:
 // CHECK:STDOUT:   return
 // CHECK:STDOUT: }
-// --- a.carbon
-fn A() {}
-
-// --- b.carbon
-fn B() {}
diff --git a/toolchain/check/testdata/basics/multifile_raw_ir.carbon b/toolchain/check/testdata/basics/multifile_raw_ir.carbon
index 9fdc4a6530ce..0a2b3f1dce0a 100644
--- a/toolchain/check/testdata/basics/multifile_raw_ir.carbon
+++ b/toolchain/check/testdata/basics/multifile_raw_ir.carbon
@@ -8,6 +8,12 @@
 //
 // AUTOUPDATE
 
+// --- a.carbon
+fn A() {}
+
+// --- b.carbon
+fn B() {}
+
 // CHECK:STDOUT: - filename: a.carbon
 // CHECK:STDOUT:   sem_ir:
 // CHECK:STDOUT:   - cross_reference_irs_size: 1
@@ -70,8 +76,3 @@
 // CHECK:STDOUT:         node+0,
 // CHECK:STDOUT:       ],
 // CHECK:STDOUT:     ]
-// --- a.carbon
-fn A() {}
-
-// --- b.carbon
-fn B() {}
diff --git a/toolchain/parse/testdata/basics/multifile.carbon b/toolchain/parse/testdata/basics/multifile.carbon
index c05a8149a871..7b9bca444add 100644
--- a/toolchain/parse/testdata/basics/multifile.carbon
+++ b/toolchain/parse/testdata/basics/multifile.carbon
@@ -4,6 +4,12 @@
 //
 // AUTOUPDATE
 
+// --- a.carbon
+fn A() {}
+
+// --- b.carbon
+fn B() {}
+
 // CHECK:STDOUT: - filename: a.carbon
 // CHECK:STDOUT:   parse_tree: [
 // CHECK:STDOUT:         {kind: 'FunctionIntroducer', text: 'fn'},
@@ -24,8 +30,3 @@
 // CHECK:STDOUT:     {kind: 'FunctionDefinition', text: '}', subtree_size: 6},
 // CHECK:STDOUT:     {kind: 'FileEnd', text: ''},
 // CHECK:STDOUT:   ]
-// --- a.carbon
-fn A() {}
-
-// --- b.carbon
-fn B() {}