diff --git a/packages/flutter_tools/lib/src/build_system/depfile.dart b/packages/flutter_tools/lib/src/build_system/depfile.dart
index a27e986e18..9d90194c93 100644
--- a/packages/flutter_tools/lib/src/build_system/depfile.dart
+++ b/packages/flutter_tools/lib/src/build_system/depfile.dart
@@ -65,16 +65,19 @@ class DepfileService {
   }
 
   void _writeFilesToBuffer(List<File> files, StringBuffer buffer) {
+    final bool backslash = _fileSystem.path.style.separator == r'\';
     for (final File outputFile in files) {
-      if (_fileSystem.path.style.separator == r'\') {
-        // backslashes and spaces in a depfile have to be escaped if the
-        // platform separator is a backslash.
-        final String path = outputFile.path.replaceAll(r'\', r'\\').replaceAll(r' ', r'\ ');
-        buffer.write(' $path');
+      String path = _fileSystem.path.normalize(outputFile.path);
+      if (backslash) {
+        // Backslashes in a depfile have to be escaped if the platform separator is a backslash.
+        path = path.replaceAll(r'\', r'\\');
       } else {
-        final String path = outputFile.path.replaceAll(r' ', r'\ ');
-        buffer.write(' $path');
+        // Convert all path separators to forward slashes.
+        path = path.replaceAll(r'\', r'/');
       }
+      // Escape spaces.
+      path = path.replaceAll(r' ', r'\ ');
+      buffer.write(' $path');
     }
   }
 
@@ -92,7 +95,8 @@ class DepfileService {
         // The tool doesn't write duplicates to these lists. This call is an attempt to
         // be resilient to the outputs of other tools which write or user edits to depfiles.
         .toSet()
-        .map(_fileSystem.file)
+        // Normalize the path before creating a file object.
+        .map((String path) => _fileSystem.file(_fileSystem.path.normalize(path)))
         .toList();
   }
 }
diff --git a/packages/flutter_tools/test/general.shard/build_system/depfile_test.dart b/packages/flutter_tools/test/general.shard/build_system/depfile_test.dart
index f0efccaf5e..3855c40141 100644
--- a/packages/flutter_tools/test/general.shard/build_system/depfile_test.dart
+++ b/packages/flutter_tools/test/general.shard/build_system/depfile_test.dart
@@ -17,6 +17,7 @@ void main() {
     fileSystem = MemoryFileSystem.test();
     depfileService = DepfileService(logger: BufferLogger.test(), fileSystem: fileSystem);
   });
+
   testWithoutContext('Can parse depfile from file', () {
     final File depfileSource = fileSystem.file('example.d')..writeAsStringSync('''
 a.txt: b.txt
@@ -48,22 +49,34 @@ a.txt c.txt d.txt: b.txt
   });
 
   testWithoutContext('Can parse depfile with windows file paths', () {
-    fileSystem = MemoryFileSystem.test(style: FileSystemStyle.windows);
-    depfileService = DepfileService(logger: BufferLogger.test(), fileSystem: fileSystem);
+    final FileSystem fileSystem = MemoryFileSystem.test(style: FileSystemStyle.windows);
+    final DepfileService depfileService = DepfileService(
+      logger: BufferLogger.test(),
+      fileSystem: fileSystem,
+    );
     final File depfileSource = fileSystem.file('example.d')..writeAsStringSync(r'''
-C:\\a.txt: C:\\b.txt
+C:\\a1.txt C:\\a2/a3.txt: C:\\b1.txt C:\\b2/b3.txt
 ''');
     final Depfile depfile = depfileService.parse(depfileSource);
 
-    expect(depfile.inputs.single.path, r'C:\b.txt');
-    expect(depfile.outputs.single.path, r'C:\a.txt');
+    expect(depfile.inputs.map((File e) => e.path).toList(), <String>[
+      r'C:\b1.txt',
+      r'C:\b2\b3.txt',
+    ]);
+    expect(depfile.outputs.map((File e) => e.path).toList(), <String>[
+      r'C:\a1.txt',
+      r'C:\a2\a3.txt',
+    ]);
   });
 
   testWithoutContext(
     'Can escape depfile with windows file paths and spaces in directory names',
     () {
-      fileSystem = MemoryFileSystem.test(style: FileSystemStyle.windows);
-      depfileService = DepfileService(logger: BufferLogger.test(), fileSystem: fileSystem);
+      final FileSystem fileSystem = MemoryFileSystem.test(style: FileSystemStyle.windows);
+      final DepfileService depfileService = DepfileService(
+        logger: BufferLogger.test(),
+        fileSystem: fileSystem,
+      );
       final File inputFile =
           fileSystem.directory(r'Hello Flutter').childFile('a.txt').absolute
             ..createSync(recursive: true);
@@ -73,8 +86,9 @@ C:\\a.txt: C:\\b.txt
       final File outputDepfile = fileSystem.file('depfile');
       depfileService.writeToFile(depfile, outputDepfile);
 
-      expect(outputDepfile.readAsStringSync(), contains(r'C:\\Hello\ Flutter\\a.txt'));
-      expect(outputDepfile.readAsStringSync(), contains(r'C:\\Hello\ Flutter\\b.txt'));
+      final String output = outputDepfile.readAsStringSync();
+      expect(output, contains(r'C:\\Hello\ Flutter\\a.txt'));
+      expect(output, contains(r'C:\\Hello\ Flutter\\b.txt'));
     },
   );
 
@@ -88,8 +102,46 @@ C:\\a.txt: C:\\b.txt
     final File outputDepfile = fileSystem.file('depfile');
     depfileService.writeToFile(depfile, outputDepfile);
 
-    expect(outputDepfile.readAsStringSync(), contains(r'/Hello\ Flutter/a.txt'));
-    expect(outputDepfile.readAsStringSync(), contains(r'/Hello\ Flutter/b.txt'));
+    final String output = outputDepfile.readAsStringSync();
+    expect(output, contains(r'/Hello\ Flutter/a.txt'));
+    expect(output, contains(r'/Hello\ Flutter/b.txt'));
+  });
+
+  testWithoutContext('Can produce normalized paths', () {
+    final List<(FileSystemStyle style, String input, String output, List<String> expects)> pairs =
+        <(FileSystemStyle style, String input, String output, List<String> expects)>[
+          (
+            FileSystemStyle.posix,
+            r'Hello Flutter\a.txt',
+            r'Hello Flutter\b.txt',
+            <String>[r'/Hello\ Flutter/a.txt', r'/Hello\ Flutter/b.txt'],
+          ),
+          (
+            FileSystemStyle.windows,
+            r'Hello Flutter/a.txt',
+            r'Hello Flutter/b.txt',
+            <String>[r'\\Hello\ Flutter\\a.txt', r'\\Hello\ Flutter\\b.txt'],
+          ),
+        ];
+
+    for (final (FileSystemStyle style, String input, String output, List<String> expects)
+        in pairs) {
+      final FileSystem fileSystem = MemoryFileSystem.test(style: style);
+      final DepfileService depfileService = DepfileService(
+        logger: BufferLogger.test(),
+        fileSystem: fileSystem,
+      );
+      final File inputFile = fileSystem.file(input).absolute..createSync(recursive: true);
+      final File outputFile = fileSystem.file(output).absolute..createSync();
+      final Depfile depfile = Depfile(<File>[inputFile], <File>[outputFile]);
+      final File outputDepfile = fileSystem.file('depfile');
+      depfileService.writeToFile(depfile, outputDepfile);
+
+      final String outputString = outputDepfile.readAsStringSync();
+      for (final String path in expects) {
+        expect(outputString, contains(path));
+      }
+    }
   });
 
   testWithoutContext('Resilient to weird whitespace', () {