diff --git a/.gitignore b/.gitignore
index 7bbbacdaa..7bbc56406 100644
--- a/.gitignore
+++ b/.gitignore
@@ -40,7 +40,7 @@ pip-log.txt
 .metadata
 .tern-project
 
-# Vim 
+# Vim
 .*.sw[a-z]
 *.un~
 Session.vim
diff --git a/src/WebAppDIRAC/Core/HandlerMgr.py b/src/WebAppDIRAC/Core/HandlerMgr.py
index 06afacc3f..ef1ce93d1 100644
--- a/src/WebAppDIRAC/Core/HandlerMgr.py
+++ b/src/WebAppDIRAC/Core/HandlerMgr.py
@@ -46,16 +46,21 @@ def getPaths(self, dirName):
     """
     pathList = []
     for extName in extensionsByPriority():
-      # TODO: Would be nicer to set these paths with setuptools metadata
-      try:
-        modFile, modPath, desc = imp.find_module(extName)
-        # to match in the real root path to enabling module web extensions (static, templates...)
-        realModPath = os.path.realpath(modPath)
-      except ImportError:
-        continue
-      staticPath = os.path.join(realModPath, "WebApp", dirName)
-      if os.path.isdir(staticPath):
-        pathList.append(staticPath)
+      if six.PY3:
+        metadata = getExtensionMetadata(extension)
+        pathList += metadata.get("web_resources", {}).get(dirName, [])
+      else:
+        # TODO: Would be nicer to set these paths with setuptools metadata
+        # FIXME: Use static_web_resources
+        try:
+          modFile, modPath, desc = imp.find_module(extName)
+          # to match in the real root path to enabling module web extensions (static, templates...)
+          realModPath = os.path.realpath(modPath)
+        except ImportError:
+          continue
+        staticPath = os.path.join(realModPath, "WebApp", dirName)
+        if os.path.isdir(staticPath):
+          pathList.append(staticPath)
     return pathList
 
   def __calculateRoutes(self):
diff --git a/src/WebAppDIRAC/__init__.py b/src/WebAppDIRAC/__init__.py
index 83f09f533..72d91e04d 100644
--- a/src/WebAppDIRAC/__init__.py
+++ b/src/WebAppDIRAC/__init__.py
@@ -38,6 +38,12 @@
 
 
 def extension_metadata():
+  import importlib.resources  # pylint: disable=no-name-in-module
+
   return {
-      "priority": 10
+      "priority": 10,
+      "web_resources": {
+          "static": [importlib.resources.files("WebAppDIRAC") / "WebApp" / "static"],
+          "template": [importlib.resources.files("WebAppDIRAC") / "WebApp" / "template"],
+      }
   }
diff --git a/src/WebAppDIRAC/scripts/dirac_webapp_run.py b/src/WebAppDIRAC/scripts/dirac_webapp_run.py
index 518950576..e9dc2234a 100755
--- a/src/WebAppDIRAC/scripts/dirac_webapp_run.py
+++ b/src/WebAppDIRAC/scripts/dirac_webapp_run.py
@@ -1,10 +1,12 @@
 #!/usr/bin/env python
-
+import os
+import six
 import sys
 import tornado
 
 from DIRAC import gConfig, S_OK
 from DIRAC.Core.Base import Script
+from DIRAC.Core.Utilities.Extensions import extensionsByPriority, getExtensionMetadata
 from DIRAC.Core.Utilities.DIRACScript import DIRACScript
 from DIRAC.ConfigurationSystem.Client.LocalConfiguration import LocalConfiguration
 from DIRAC.FrameworkSystem.Client.Logger import gLogger
@@ -14,6 +16,48 @@
 __RCSID__ = "$Id$"
 
 
+def _createStaticSymlinks(targetDir):
+  """Create symlinks to static web content
+
+  This method is used to populate the directory specified in the local
+  configuration under ``/WebApp/StaticResourceLinkDir`` so that nginx can
+  serve this content from a consistent location.
+
+  :params str targetDir: The directory in which to create the symlinks
+  """
+  extensions = extensionsByPriority()
+  for extension in extensions:
+    if six.PY3:
+      metadata = getExtensionMetadata(extension)
+      staticDirs = metadata.get("web_resources", {}).get("static", [])
+    else:
+      staticDirs = []
+      try:
+        modFile, modPath, desc = imp.find_module(extName)
+        # to match in the real root path to enabling module web extensions (static, templates...)
+        realModPath = os.path.realpath(modPath)
+      except ImportError:
+        continue
+      staticDirs = [os.path.join(realModPath, "WebApp", "static")]
+      if not os.path.isdir(staticDirs[0]):
+        continue
+
+    for i, path in enumerate(sorted(staticDirs)):
+      destination = os.path.join(targetDir, extension)
+      # If there is more than one suffix append a counter
+      if i >= 1:
+        destination += "-%s" % i
+      gLogger.notice("    creating symlink from", "%s to %s" % (path, destination))
+      if os.path.islink(destination):
+        if path == os.readlink(destination):
+          # The link is already up to date
+          continue
+        os.unlink(destination)
+      os.symlink(path, destination)
+
+  # TODO: Check /etc/nginx/conf.d/site.conf and warn if it's inconsistent?
+
+
 @DIRACScript()
 def main():
   def disableDevMode(op):
@@ -44,6 +88,13 @@ def setHandlers(op):
     gLogger.fatal("There were errors when loading configuration", result['Message'])
     sys.exit(1)
 
+  result = DIRAC.gConfig.getOption("/WebApp/StaticResourceLinkDir")
+  if result["OK"]:
+    gLogger.notice("Creating symlinks to static resources")
+    _createStaticSymlinks(result["Value"])
+  else:
+    gLogger.warn("Not creating symlinks to static resources", result["Message"])
+
   gLogger.notice("Set next path(s): ", localCfg.handlersLoc)
   app = App(handlersLoc=localCfg.handlersLoc)
   result = app.bootstrap()