diff --git a/starlette/staticfiles.py b/starlette/staticfiles.py
index d5964158..b816fb1b 100644
--- a/starlette/staticfiles.py
+++ b/starlette/staticfiles.py
@@ -5,46 +5,85 @@ import stat
 
 
 class StaticFile:
-    def __init__(self, *, path):
+    def __init__(self, path):
         self.path = path
 
     def __call__(self, scope):
         if scope['method'] not in ('GET', 'HEAD'):
             return PlainTextResponse('Method not allowed', status_code=406)
-        return _StaticFileResponder(scope, path=self.path, allow_404=False)
+        return _StaticFileResponder(scope, path=self.path)
 
 
 class StaticFiles:
     def __init__(self, *, directory):
         self.directory = directory
+        self.config_checked = False
 
     def __call__(self, scope):
         if scope['method'] not in ('GET', 'HEAD'):
             return PlainTextResponse('Method not allowed', status_code=406)
         split_path = scope['path'].split('/')
         path = os.path.join(self.directory, *split_path)
-        return _StaticFileResponder(scope, path=path, allow_404=True)
+        if self.config_checked:
+            check_directory = None
+        else:
+            check_directory = self.directory
+            self.config_checked = True
+        return _StaticFilesResponder(scope, path=path, check_directory=check_directory)
 
 
 class _StaticFileResponder:
-    def __init__(self, scope, path, allow_404):
+    def __init__(self, scope, path):
         self.scope = scope
         self.path = path
-        self.allow_404 = allow_404
 
     async def __call__(self, receive, send):
         try:
             stat_result = await aio_stat(self.path)
         except FileNotFoundError:
-            if not self.allow_404:
-                raise RuntimeError("StaticFile at path '%s' does not exist." % self.path)
+            raise RuntimeError("StaticFile at path '%s' does not exist." % self.path)
+        else:
+            mode = stat_result.st_mode
+            if not stat.S_ISREG(mode):
+                raise RuntimeError("StaticFile at path '%s' is not a file." % self.path)
+
+        response = FileResponse(self.path, stat_result=stat_result)
+        await response(receive, send)
+
+
+class _StaticFilesResponder:
+    def __init__(self, scope, path, check_directory=None):
+        self.scope = scope
+        self.path = path
+        self.check_directory = check_directory
+
+    async def check_directory_configured_correctly(self):
+        """
+        Perform a one-off configuration check that StaticFiles is actually
+        pointed at a directory, so that we can raise loud errors rather than
+        just returning 404 responses.
+        """
+        directory = self.check_directory
+        try:
+            stat_result = await aio_stat(directory)
+        except FileNotFoundError:
+            raise RuntimeError("StaticFiles directory '%s' does not exist." % directory)
+        if not stat.S_ISDIR(stat_result.st_mode):
+            raise RuntimeError("StaticFiles path '%s' is not a directory." % directory)
+
+    async def __call__(self, receive, send):
+        if self.check_directory is not None:
+            await self.check_directory_configured_correctly()
+
+        try:
+            stat_result = await aio_stat(self.path)
+        except FileNotFoundError:
             response = PlainTextResponse('Not found', status_code=404)
         else:
             mode = stat_result.st_mode
-            if stat.S_ISREG(mode) or stat.S_ISLNK(mode):
-                response = FileResponse(self.path, stat_result=stat_result)
-            else:
-                if not self.allow_404:
-                    raise RuntimeError("StaticFile at path '%s' is not a file." % self.path)
+            if not stat.S_ISREG(mode):
                 response = PlainTextResponse('Not found', status_code=404)
+            else:
+                response = FileResponse(self.path, stat_result=stat_result)
+
         await response(receive, send)
diff --git a/tests/test_staticfiles.py b/tests/test_staticfiles.py
index 5565a432..75e072d4 100644
--- a/tests/test_staticfiles.py
+++ b/tests/test_staticfiles.py
@@ -91,3 +91,34 @@ def test_staticfiles_with_missing_file_returns_404(tmpdir):
     response = client.get("/404.txt")
     assert response.status_code == 404
     assert response.text == 'Not found'
+
+
+def test_staticfiles_configured_with_missing_directory(tmpdir):
+    path = os.path.join(tmpdir, "no_such_directory")
+    app = StaticFiles(directory=path)
+    client = TestClient(app)
+    with pytest.raises(RuntimeError) as exc:
+        response = client.get("/example.txt")
+    assert 'does not exist' in str(exc)
+
+
+def test_staticfiles_configured_with_file_instead_of_directory(tmpdir):
+    path = os.path.join(tmpdir, "example.txt")
+    with open(path, "w") as file:
+        file.write("<file content>")
+
+    app = StaticFiles(directory=path)
+    client = TestClient(app)
+    with pytest.raises(RuntimeError) as exc:
+        response = client.get("/example.txt")
+    assert 'is not a directory' in str(exc)
+
+
+def test_staticfiles_config_check_occurs_only_once(tmpdir):
+    app = StaticFiles(directory=tmpdir)
+    client = TestClient(app)
+    assert not app.config_checked
+    response = client.get("/")
+    assert app.config_checked
+    response = client.get("/")
+    assert app.config_checked