diff --git a/python/mozbuild/mozbuild/backend/common.py b/python/mozbuild/mozbuild/backend/common.py
index 19197427022a..cc8e74be800a 100644
--- a/python/mozbuild/mozbuild/backend/common.py
+++ b/python/mozbuild/mozbuild/backend/common.py
@@ -175,9 +175,9 @@ class TestManager(object):
         self.tests_by_path = defaultdict(list)
         self.installs_by_path = defaultdict(list)
         self.deferred_installs = set()
-        self.manifest_default_support_files = {}
+        self.manifest_defaults = {}
 
-    def add(self, t, flavor, topsrcdir, default_supp_files):
+    def add(self, t, flavor, topsrcdir):
         t = dict(t)
         t['flavor'] = flavor
 
@@ -188,19 +188,14 @@ class TestManager(object):
         t['file_relpath'] = key
         t['dir_relpath'] = mozpath.dirname(key)
 
-        # Support files are propagated from the default section to individual
-        # tests by the manifest parser, but we end up storing a lot of
-        # redundant data due to the huge number of support files.
-        # So if we have support files that are the same as the manifest default
-        # we track that separately, per-manifest instead of per-test, to save
-        # space.
-        supp_files = t.get('support-files')
-        if supp_files and supp_files == default_supp_files:
-            self.manifest_default_support_files[t['manifest']] = default_supp_files
-            del t['support-files']
-
         self.tests_by_path[key].append(t)
 
+    def add_defaults(self, manifest):
+        if not hasattr(manifest, 'manifest_defaults'):
+            return
+        for sub_manifest, defaults in manifest.manifest_defaults.items():
+            self.manifest_defaults[sub_manifest] = defaults
+
     def add_installs(self, obj, topsrcdir):
         for src, (dest, _) in obj.installs.iteritems():
             key = src[len(topsrcdir)+1:]
@@ -236,8 +231,8 @@ class CommonBackend(BuildBackend):
 
         if isinstance(obj, TestManifest):
             for test in obj.tests:
-                self._test_manager.add(test, obj.flavor, obj.topsrcdir,
-                                       obj.default_support_files)
+                self._test_manager.add(test, obj.flavor, obj.topsrcdir)
+            self._test_manager.add_defaults(obj.manifest)
             self._test_manager.add_installs(obj, obj.topsrcdir)
 
         elif isinstance(obj, XPIDLFile):
@@ -376,8 +371,10 @@ class CommonBackend(BuildBackend):
         # Write out a machine-readable file describing every test.
         topobjdir = self.environment.topobjdir
         with self._write_file(mozpath.join(topobjdir, 'all-tests.json')) as fh:
-            json.dump([self._test_manager.tests_by_path,
-                       self._test_manager.manifest_default_support_files], fh)
+            json.dump(self._test_manager.tests_by_path, fh)
+
+        with self._write_file(mozpath.join(topobjdir, 'test-defaults.json')) as fh:
+            json.dump(self._test_manager.manifest_defaults, fh)
 
         path = mozpath.join(self.environment.topobjdir, 'test-installs.json')
         with self._write_file(path) as fh:
diff --git a/python/mozbuild/mozbuild/frontend/data.py b/python/mozbuild/mozbuild/frontend/data.py
index e26f0851c641..fdf8cca17221 100644
--- a/python/mozbuild/mozbuild/frontend/data.py
+++ b/python/mozbuild/mozbuild/frontend/data.py
@@ -642,11 +642,6 @@ class TestManifest(ContextDerived):
         # If this manifest is a duplicate of another one, this is the
         # manifestparser.TestManifest of the other one.
         'dupe_manifest',
-
-        # The support files appearing in the DEFAULT section of this
-        # manifest. This enables a space optimization in all-tests.json,
-        # see the comment in mozbuild/backend/common.py.
-        'default_support_files',
     )
 
     def __init__(self, context, path, manifest, flavor=None,
@@ -668,7 +663,6 @@ class TestManifest(ContextDerived):
         self.tests = []
         self.external_installs = set()
         self.deferred_installs = set()
-        self.default_support_files = None
 
 
 class LocalInclude(ContextDerived):
diff --git a/python/mozbuild/mozbuild/frontend/emitter.py b/python/mozbuild/mozbuild/frontend/emitter.py
index 0dd1da9ac292..52f571867200 100644
--- a/python/mozbuild/mozbuild/frontend/emitter.py
+++ b/python/mozbuild/mozbuild/frontend/emitter.py
@@ -1200,18 +1200,16 @@ class TreeMetadataEmitter(LoggingMixin):
         install_prefix = mozpath.join(install_root, install_subdir)
 
         try:
-            defaults = mpmanifest.manifest_defaults[os.path.normpath(path)]
             if not mpmanifest.tests:
                 raise SandboxValidationError('Empty test manifest: %s'
                     % path, context)
 
+            defaults = mpmanifest.manifest_defaults[os.path.normpath(path)]
             obj = TestManifest(context, path, mpmanifest, flavor=flavor,
                 install_prefix=install_prefix,
                 relpath=mozpath.join(manifest_reldir, mozpath.basename(path)),
                 dupe_manifest='dupe-manifest' in defaults)
 
-            obj.default_support_files = defaults.get('support-files')
-
             filtered = mpmanifest.tests
 
             # Jetpack add-on tests are expected to be generated during the
@@ -1263,6 +1261,9 @@ class TreeMetadataEmitter(LoggingMixin):
 
                 process_support_files(test)
 
+            for path, m_defaults in mpmanifest.manifest_defaults.items():
+                process_support_files(m_defaults)
+
             # We also copy manifests into the output directory,
             # including manifests from [include:foo] directives.
             for mpath in mpmanifest.manifests():
@@ -1281,8 +1282,8 @@ class TreeMetadataEmitter(LoggingMixin):
                     del obj.installs[mozpath.join(manifest_dir, f)]
                 except KeyError:
                     raise SandboxValidationError('Error processing test '
-                       'manifest %s: entry in generated-files not present '
-                       'elsewhere in manifest: %s' % (path, f), context)
+                        'manifest %s: entry in generated-files not present '
+                        'elsewhere in manifest: %s' % (path, f), context)
 
             yield obj
         except (AssertionError, Exception):
diff --git a/python/mozbuild/mozbuild/test/backend/test_recursivemake.py b/python/mozbuild/mozbuild/test/backend/test_recursivemake.py
index 683cd5275d97..df4fa958d3eb 100644
--- a/python/mozbuild/mozbuild/test/backend/test_recursivemake.py
+++ b/python/mozbuild/mozbuild/test/backend/test_recursivemake.py
@@ -528,7 +528,7 @@ class TestRecursiveMakeBackend(BackendTester):
         self.assertTrue(os.path.exists(all_tests_path))
 
         with open(all_tests_path, 'rt') as fh:
-            o, _ = json.load(fh)
+            o = json.load(fh)
 
             self.assertIn('xpcshell.js', o)
             self.assertIn('dir1/test_bar.js', o)
@@ -854,8 +854,7 @@ class TestRecursiveMakeBackend(BackendTester):
         self.assertTrue(os.path.exists(all_tests_path))
 
         with open(all_tests_path, 'rt') as fh:
-            o, _ = json.load(fh)
-
+            o = json.load(fh)
             self.assertIn('mochitest.js', o)
             self.assertIn('not_packaged.java', o)
 
diff --git a/python/mozbuild/mozbuild/test/frontend/data/test-manifest-dupes/mochitest.ini b/python/mozbuild/mozbuild/test/frontend/data/test-manifest-dupes/mochitest.ini
index 237f5c383097..2f1fc406a05b 100644
--- a/python/mozbuild/mozbuild/test/frontend/data/test-manifest-dupes/mochitest.ini
+++ b/python/mozbuild/mozbuild/test/frontend/data/test-manifest-dupes/mochitest.ini
@@ -2,7 +2,6 @@
 # http://creativecommons.org/publicdomain/zero/1.0/
 
 [DEFAULT]
-support-files = foo.js bar.js
+support-files = bar.js foo.js bar.js
 
 [test_baz.js]
-support-files = bar.js
\ No newline at end of file
diff --git a/python/mozbuild/mozbuild/test/test_testing.py b/python/mozbuild/mozbuild/test/test_testing.py
index 76c769e5f5ab..853109413482 100644
--- a/python/mozbuild/mozbuild/test/test_testing.py
+++ b/python/mozbuild/mozbuild/test/test_testing.py
@@ -22,7 +22,7 @@ from mozbuild.testing import (
 
 
 ALL_TESTS_JSON = b'''
-[{
+{
     "accessible/tests/mochitest/actions/test_anchors.html": [
         {
             "dir_relpath": "accessible/tests/mochitest/actions",
@@ -154,9 +154,11 @@ ALL_TESTS_JSON = b'''
             "tags": "devtools"
         }
    ]
-}, {
-   "/Users/gps/src/firefox/toolkit/mozapps/update/test/unit/xpcshell_updater.ini": "\\ndata/**\\nxpcshell_updater.ini"
-}]'''.strip()
+}'''.strip()
+
+TEST_DEFAULTS = b'''{
+    "/Users/gps/src/firefox/toolkit/mozapps/update/test/unit/xpcshell_updater.ini": {"support-files": "\\ndata/**\\nxpcshell_updater.ini"}
+}'''
 
 
 class Base(unittest.TestCase):
@@ -170,12 +172,17 @@ class Base(unittest.TestCase):
         self._temp_files = []
 
     def _get_test_metadata(self):
-        f = NamedTemporaryFile()
-        f.write(ALL_TESTS_JSON)
-        f.flush()
-        self._temp_files.append(f)
+        all_tests = NamedTemporaryFile()
+        all_tests.write(ALL_TESTS_JSON)
+        all_tests.flush()
+        self._temp_files.append(all_tests)
 
-        return TestMetadata(filename=f.name)
+        test_defaults = NamedTemporaryFile()
+        test_defaults.write(TEST_DEFAULTS)
+        test_defaults.flush()
+        self._temp_files.append(test_defaults)
+
+        return TestMetadata(all_tests.name, test_defaults=test_defaults.name)
 
 
 class TestTestMetadata(Base):
@@ -246,6 +253,8 @@ class TestTestResolver(Base):
 
         with open(os.path.join(topobjdir, 'all-tests.json'), 'wt') as fh:
             fh.write(ALL_TESTS_JSON)
+        with open(os.path.join(topobjdir, 'test-defaults.json'), 'wt') as fh:
+            fh.write(TEST_DEFAULTS)
 
         o = MozbuildObject(self.FAKE_TOPSRCDIR, None, None, topobjdir=topobjdir)
 
diff --git a/python/mozbuild/mozbuild/testing.py b/python/mozbuild/mozbuild/testing.py
index 099fcbc43966..ac891d4b9c98 100644
--- a/python/mozbuild/mozbuild/testing.py
+++ b/python/mozbuild/mozbuild/testing.py
@@ -51,30 +51,29 @@ class TestMetadata(object):
     configuration.
     """
 
-    def __init__(self, filename=None):
+    def __init__(self, all_tests, test_defaults=None):
         self._tests_by_path = OrderedDefaultDict(list)
         self._tests_by_flavor = defaultdict(set)
         self._test_dirs = set()
 
-        if filename:
-            with open(filename, 'rt') as fh:
-                test_data, manifest_support_files = json.load(fh)
-
-                for path, tests in test_data.items():
-                    for metadata in tests:
-                        # Many tests inherit their "support-files" from a manifest
-                        # level default, so we store these separately to save
-                        # disk space, and propagate them to each test when
-                        # de-serializing here.
-                        manifest = metadata['manifest']
-                        support_files = manifest_support_files.get(manifest)
-                        if support_files and 'support-files' not in metadata:
-                            metadata['support-files'] = support_files
-                        self._tests_by_path[path].append(metadata)
-                        self._test_dirs.add(os.path.dirname(path))
-
-                        flavor = metadata.get('flavor')
-                        self._tests_by_flavor[flavor].add(path)
+        with open(all_tests, 'rt') as fh:
+            test_data = json.load(fh)
+        defaults = None
+        if test_defaults:
+            with open(test_defaults, 'rt') as fh:
+                defaults = json.load(fh)
+        for path, tests in test_data.items():
+            for metadata in tests:
+                if defaults:
+                    manifest = metadata['manifest']
+                    manifest_defaults = defaults.get(manifest)
+                    if manifest_defaults:
+                        metadata = manifestparser.combine_fields(manifest_defaults,
+                                                                 metadata)
+                self._tests_by_path[path].append(metadata)
+                self._test_dirs.add(os.path.dirname(path))
+                flavor = metadata.get('flavor')
+                self._tests_by_flavor[flavor].add(path)
 
     def tests_with_flavor(self, flavor):
         """Obtain all tests having the specified flavor.
@@ -183,8 +182,11 @@ class TestResolver(MozbuildObject):
         self._run_make(target='run-tests-deps', pass_thru=True,
                        print_directory=False)
 
-        self._tests = TestMetadata(filename=os.path.join(self.topobjdir,
-            'all-tests.json'))
+        self._tests = TestMetadata(os.path.join(self.topobjdir,
+                                                'all-tests.json'),
+                                   test_defaults=os.path.join(self.topobjdir,
+                                                              'test-defaults.json'))
+
         self._test_rewrites = {
             'a11y': os.path.join(self.topobjdir, '_tests', 'testing',
                 'mochitest', 'a11y'),
@@ -503,7 +505,8 @@ def read_manifestparser_manifest(context, manifest_path):
     path = mozpath.normpath(mozpath.join(context.srcdir, manifest_path))
     return manifestparser.TestManifest(manifests=[path], strict=True,
                                        rootdir=context.config.topsrcdir,
-                                       finder=context._finder)
+                                       finder=context._finder,
+                                       handle_defaults=False)
 
 def read_reftest_manifest(context, manifest_path):
     import reftest