diff --git a/.flake8 b/.flake8
index 4c64cd4eada0..0103d1ff3001 100644
--- a/.flake8
+++ b/.flake8
@@ -42,7 +42,7 @@ per-file-ignores =
     matplotlib/backends/qt_editor/formlayout.py: E301, E501
     matplotlib/backends/tkagg.py: E231, E302, E701
     matplotlib/backends/windowing.py: E301, E302
-    matplotlib/font_manager.py: E203, E221, E225, E251, E261, E262, E302, E501
+    matplotlib/font_manager.py: E203, E221, E251, E261, E262, E302, E501
     matplotlib/fontconfig_pattern.py: E201, E203, E221, E222, E225, E302
     matplotlib/legend_handler.py: E201, E501
     matplotlib/mathtext.py: E201, E202, E203, E211, E221, E222, E225, E231, E251, E261, E301, E302, E303, E402, E501
diff --git a/lib/matplotlib/font_manager.py b/lib/matplotlib/font_manager.py
index b8688860c9d4..e451dfdb281f 100644
--- a/lib/matplotlib/font_manager.py
+++ b/lib/matplotlib/font_manager.py
@@ -44,6 +44,7 @@
     from dummy_threading import Timer
 import warnings
 
+import matplotlib as mpl
 from matplotlib import afm, cbook, ft2font, rcParams, get_cachedir
 from matplotlib.fontconfig_pattern import (
     parse_fontconfig_pattern, generate_fontconfig_pattern)
@@ -828,15 +829,23 @@ def copy(self):
 class JSONEncoder(json.JSONEncoder):
     def default(self, o):
         if isinstance(o, FontManager):
-            return dict(o.__dict__, _class='FontManager')
+            return dict(o.__dict__, __class__='FontManager')
         elif isinstance(o, FontEntry):
-            return dict(o.__dict__, _class='FontEntry')
+            d = dict(o.__dict__, __class__='FontEntry')
+            try:
+                # Cache paths of fonts shipped with mpl relative to the mpl
+                # data path, which helps in the presence of venvs.
+                d["fname"] = str(
+                    Path(d["fname"]).relative_to(mpl.get_data_path()))
+            except ValueError:
+                pass
+            return d
         else:
             return super().default(o)
 
 
 def _json_decode(o):
-    cls = o.pop('_class', None)
+    cls = o.pop('__class__', None)
     if cls is None:
         return o
     elif cls == 'FontManager':
@@ -846,15 +855,21 @@ def _json_decode(o):
     elif cls == 'FontEntry':
         r = FontEntry.__new__(FontEntry)
         r.__dict__.update(o)
+        if not os.path.isabs(r.fname):
+            r.fname = os.path.join(mpl.get_data_path(), r.fname)
         return r
     else:
-        raise ValueError("don't know how to deserialize _class=%s" % cls)
+        raise ValueError("don't know how to deserialize __class__=%s" % cls)
 
 
 def json_dump(data, filename):
-    """Dumps a data structure as JSON in the named file.
-    Handles FontManager and its fields."""
+    """
+    Dumps a data structure as JSON in the named file.
 
+    Handles FontManager and its fields.  File paths that are children of the
+    Matplotlib data path (typically, fonts shipped with Matplotlib) are stored
+    relative to that data path (to remain valid across virtualenvs).
+    """
     with open(filename, 'w') as fh:
         try:
             json.dump(data, fh, cls=JSONEncoder, indent=2)
@@ -863,9 +878,13 @@ def json_dump(data, filename):
 
 
 def json_load(filename):
-    """Loads a data structure as JSON from the named file.
-    Handles FontManager and its fields."""
+    """
+    Loads a data structure as JSON from the named file.
 
+    Handles FontManager and its fields.  Relative file paths are interpreted
+    as being relative to the Matplotlib data path, and transformed into
+    absolute paths.
+    """
     with open(filename, 'r') as fh:
         return json.load(fh, object_hook=_json_decode)
 
@@ -926,7 +945,7 @@ class FontManager(object):
     # Increment this version number whenever the font cache data
     # format or behavior has changed and requires a existing font
     # cache files to be rebuilt.
-    __version__ = 201
+    __version__ = 300
 
     def __init__(self, size=None, weight='normal'):
         self._version = self.__version__
@@ -951,30 +970,32 @@ def __init__(self, size=None, weight='normal'):
         _log.debug('font search path %s', str(paths))
         #  Load TrueType fonts and create font dictionary.
 
-        self.ttffiles = findSystemFonts(paths) + findSystemFonts()
         self.defaultFamily = {
             'ttf': 'DejaVu Sans',
             'afm': 'Helvetica'}
         self.defaultFont = {}
 
-        for fname in self.ttffiles:
-            _log.debug('trying fontname %s', fname)
-            if fname.lower().find('DejaVuSans.ttf')>=0:
-                self.defaultFont['ttf'] = fname
-                break
-        else:
-            # use anything
-            self.defaultFont['ttf'] = self.ttffiles[0]
+        ttffiles = findSystemFonts(paths) + findSystemFonts()
+        self.defaultFont['ttf'] = next(
+            (fname for fname in ttffiles
+             if fname.lower().endswith("dejavusans.ttf")),
+            ttffiles[0])
+        self.ttflist = createFontList(ttffiles)
 
-        self.ttflist = createFontList(self.ttffiles)
+        afmfiles = (findSystemFonts(paths, fontext='afm')
+                    + findSystemFonts(fontext='afm'))
+        self.afmlist = createFontList(afmfiles, fontext='afm')
+        self.defaultFont['afm'] = afmfiles[0] if afmfiles else None
 
-        self.afmfiles = (findSystemFonts(paths, fontext='afm')
-                         + findSystemFonts(fontext='afm'))
-        self.afmlist = createFontList(self.afmfiles, fontext='afm')
-        if len(self.afmfiles):
-            self.defaultFont['afm'] = self.afmfiles[0]
-        else:
-            self.defaultFont['afm'] = None
+    @property
+    @cbook.deprecated("3.0")
+    def ttffiles(self):
+        return [font.fname for font in self.ttflist]
+
+    @property
+    @cbook.deprecated("3.0")
+    def afmfiles(self):
+        return [font.fname for font in self.afmlist]
 
     def get_default_weight(self):
         """
@@ -1312,7 +1333,8 @@ def findfont(prop, fontext='ttf'):
 
     cachedir = get_cachedir()
     if cachedir is not None:
-        _fmcache = os.path.join(cachedir, 'fontList.json')
+        _fmcache = os.path.join(
+            cachedir, 'fontlist-v{}.json'.format(FontManager.__version__))
 
     fontManager = None