diff --git a/whitenoise/base.py b/whitenoise/base.py
index 16d6d5bb..45d02da5 100644
--- a/whitenoise/base.py
+++ b/whitenoise/base.py
@@ -96,18 +96,31 @@ def serve(static_file, environ, start_response):
             return file_wrapper(response.file)
         else:
             return []
+    
+    def normalize_root(self, root):
+        value = decode_if_byte_string(root, force_text=True)
+        value = os.path.abspath(value)
+        value = value.rstrip(os.path.sep) + os.path.sep
+        return value
+    
+    def normalize_prefix(self, prefix):
+        value = decode_if_byte_string(prefix)
+        value = ensure_leading_trailing_slash(value)
+        return value
+    
+    def insert_directory(self, root, prefix):
+        root = self.normalize_root(root)
+        prefix = self.normalize_prefix(prefix)
+        self.directories.insert(0, (root, prefix))
 
     def add_files(self, root, prefix=None):
-        root = decode_if_byte_string(root, force_text=True)
-        root = os.path.abspath(root)
-        root = root.rstrip(os.path.sep) + os.path.sep
-        prefix = decode_if_byte_string(prefix)
-        prefix = ensure_leading_trailing_slash(prefix)
+        root = self.normalize_root(root)
+        prefix = self.normalize_prefix(prefix)
         if self.autorefresh:
             # Later calls to `add_files` overwrite earlier ones, hence we need
             # to store the list of directories in reverse order so later ones
             # match first when they're checked in "autorefresh" mode
-            self.directories.insert(0, (root, prefix))
+            self.insert_directory(root, prefix)
         else:
             if os.path.isdir(root):
                 self.update_files_dictionary(root, prefix)
diff --git a/whitenoise/middleware.py b/whitenoise/middleware.py
index feec8a31..0a8d431f 100644
--- a/whitenoise/middleware.py
+++ b/whitenoise/middleware.py
@@ -1,18 +1,27 @@
+import logging
 import os
+from itertools import chain
 from posixpath import basename
 from urllib.parse import urlparse
 
 from django.conf import settings
-from django.contrib.staticfiles.storage import staticfiles_storage
+from django.contrib.staticfiles.storage import staticfiles_storage, ManifestStaticFilesStorage
 from django.contrib.staticfiles import finders
 from django.http import FileResponse
 from django.urls import get_script_prefix
+from django.utils.functional import cached_property
 
 from .base import WhiteNoise
 from .string_utils import decode_if_byte_string, ensure_leading_trailing_slash
 
 
-__all__ = ["WhiteNoiseMiddleware"]
+__all__ = [
+    "WhiteNoiseMiddleware",
+    "LazyWhiteNoiseMiddleware",
+]
+
+
+logger = logging.getLogger(__name__)
 
 
 class WhiteNoiseFileResponse(FileResponse):
@@ -40,6 +49,7 @@ class WhiteNoiseMiddleware(WhiteNoise):
     root = None
     use_finders = False
     static_prefix = None
+    add_static_root_files = True
 
     def __init__(self, get_response=None, settings=settings):
         self.get_response = get_response
@@ -47,12 +57,18 @@ def __init__(self, get_response=None, settings=settings):
         # Pass None for `application`
         super(WhiteNoiseMiddleware, self).__init__(None)
         if self.static_root:
-            self.add_files(self.static_root, prefix=self.static_prefix)
+            if self.add_static_root_files:
+                self.add_files(self.static_root, prefix=self.static_prefix)
+            else:
+                self.insert_directory(self.static_root, self.static_prefix)
         if self.root:
             self.add_files(self.root)
         if self.use_finders and not self.autorefresh:
             self.add_files_from_finders()
 
+    def can_lazy_load_url(self, url):
+        return False
+
     def __call__(self, request):
         response = self.process_request(request)
         if response is None:
@@ -64,6 +80,11 @@ def process_request(self, request):
             static_file = self.find_file(request.path_info)
         else:
             static_file = self.files.get(request.path_info)
+            if static_file is None and self.can_lazy_load_url(request.path_info):
+                static_file = self.find_file(request.path_info)
+                if static_file is not None:
+                    logger.info('Lazy loaded %s', request.path_info)
+                    self.files[request.path_info] = static_file
         if static_file is not None:
             return self.serve(static_file, request)
 
@@ -168,3 +189,20 @@ def get_static_url(self, name):
             return decode_if_byte_string(staticfiles_storage.url(name))
         except ValueError:
             return None
+
+
+class LazyWhiteNoiseMiddleware(WhiteNoiseMiddleware):
+    add_static_root_files = False
+
+    @cached_property
+    def known_static_urls(self):
+        if isinstance(staticfiles_storage, ManifestStaticFilesStorage):
+            serve_unhashed = not getattr(settings, "WHITENOISE_KEEP_ONLY_HASHED_FILES", False)
+            return set(['{}{}'.format(self.static_prefix, n) for n in chain(
+                staticfiles_storage.hashed_files.values(),
+                staticfiles_storage.hashed_files.keys() if serve_unhashed else [],
+            )])
+
+    def can_lazy_load_url(self, url):
+        return url.startswith(self.static_prefix) and \
+            self.known_static_urls is None or url in self.known_static_urls