diff --git a/doc/source/admin/galaxy_options.rst b/doc/source/admin/galaxy_options.rst
index 539375070e7..1ca46ebcb9e 100644
--- a/doc/source/admin/galaxy_options.rst
+++ b/doc/source/admin/galaxy_options.rst
@@ -2502,9 +2502,9 @@
 
 :Description:
     Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    it via a proxy server. You can use these paths (or ones in the
+    proxy server) to point to your own styles. The static_* options
+    that refer to paths are relative to the current working directory.
 :Default: ``true``
 :Type: bool
 
@@ -2514,10 +2514,8 @@
 ~~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    Value of cache time for static content served by Galaxy. Ignored
+    if static_enabled is false.
 :Default: ``360``
 :Type: int
 
@@ -2527,24 +2525,32 @@
 ~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    Path to the static content dir. Ignored if static_enabled is
+    false.
 :Default: ``static/``
 :Type: str
 
 
+~~~~~~~~~~~~~~~~~~~
+``static_dist_dir``
+~~~~~~~~~~~~~~~~~~~
+
+:Description:
+    Path to the built Galaxy client application, static/dist/ in the
+    Galaxy source code after the build is complete. Ignored if
+    static_enabled is false.
+:Default: ``static/dist/``
+:Type: str
+
+
 ~~~~~~~~~~~~~~~~~~~~~
 ``static_images_dir``
 ~~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
-:Default: ``static/images``
+    Path to the static images directory. Ignored if static_enabled is
+    false.
+:Default: ``static/images/``
 :Type: str
 
 
@@ -2553,10 +2559,8 @@
 ~~~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    Path to favicon.ico, not the directory that contains it (the name
+    is a misnomer). Ignored if static_enabled is false.
 :Default: ``static/favicon.ico``
 :Type: str
 
@@ -2566,10 +2570,8 @@
 ~~~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    Path to the static scripts directory. Ignored if static_enabled is
+    false.
 :Default: ``static/scripts/``
 :Type: str
 
@@ -2579,11 +2581,9 @@
 ~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
-:Default: ``static/style``
+    Path to the static style directory. Ignored if static_enabled is
+    false.
+:Default: ``static/style/``
 :Type: str
 
 
@@ -2592,10 +2592,7 @@
 ~~~~~~~~~~~~~~~~~~~~~
 
 :Description:
-    Serve static content, which must be enabled if you're not serving
-    it via a proxy server.  These options should be self explanatory
-    and so are not documented individually.  You can use these paths
-    (or ones in the proxy server) to point to your own styles.
+    Path to robots.txt. Ignored if static_enabled is false.
 :Default: ``static/robots.txt``
 :Type: str
 
diff --git a/lib/galaxy/config/sample/galaxy.yml.sample b/lib/galaxy/config/sample/galaxy.yml.sample
index 27f517a2e4b..7f5da5718ff 100644
--- a/lib/galaxy/config/sample/galaxy.yml.sample
+++ b/lib/galaxy/config/sample/galaxy.yml.sample
@@ -1533,51 +1533,40 @@ galaxy:
   #terms_url: null
 
   # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # via a proxy server. You can use these paths (or ones in the proxy
+  # server) to point to your own styles. The static_* options that refer
+  # to paths are relative to the current working directory.
   #static_enabled: true
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # Value of cache time for static content served by Galaxy. Ignored if
+  # static_enabled is false.
   #static_cache_time: 360
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # Path to the static content dir. Ignored if static_enabled is false.
   #static_dir: static/
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
-  #static_images_dir: static/images
+  # Path to the built Galaxy client application, static/dist/ in the
+  # Galaxy source code after the build is complete. Ignored if
+  # static_enabled is false.
+  #static_dist_dir: static/dist/
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # Path to the static images directory. Ignored if static_enabled is
+  # false.
+  #static_images_dir: static/images/
+
+  # Path to favicon.ico, not the directory that contains it (the name is
+  # a misnomer). Ignored if static_enabled is false.
   #static_favicon_dir: static/favicon.ico
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # Path to the static scripts directory. Ignored if static_enabled is
+  # false.
   #static_scripts_dir: static/scripts/
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
-  #static_style_dir: static/style
+  # Path to the static style directory. Ignored if static_enabled is
+  # false.
+  #static_style_dir: static/style/
 
-  # Serve static content, which must be enabled if you're not serving it
-  # via a proxy server.  These options should be self explanatory and so
-  # are not documented individually.  You can use these paths (or ones
-  # in the proxy server) to point to your own styles.
+  # Path to robots.txt. Ignored if static_enabled is false.
   #static_robots_txt: static/robots.txt
 
   # Incremental Display Options
diff --git a/lib/galaxy/config/schemas/config_schema.yml b/lib/galaxy/config/schemas/config_schema.yml
index e798a0a310d..98b49e587f5 100644
--- a/lib/galaxy/config/schemas/config_schema.yml
+++ b/lib/galaxy/config/schemas/config_schema.yml
@@ -1866,19 +1866,17 @@ mapping:
         required: false
         desc: |
           Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          proxy server. You can use these paths (or ones in the proxy server) to point to
+          your own styles. The static_* options that refer to paths are relative to the
+          current working directory.
 
       static_cache_time:
         type: int
         default: 360
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Value of cache time for static content served by Galaxy. Ignored if
+          static_enabled is false.
 
       static_dir:
         type: str
@@ -1886,21 +1884,24 @@ mapping:
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to the static content dir. Ignored if static_enabled is false.
 
-      static_images_dir:
+      static_dist_dir:
         type: str
-        default: static/images
+        default: static/dist/
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to the built Galaxy client application, static/dist/ in the Galaxy source
+          code after the build is complete. Ignored if static_enabled is false.
+
+      static_images_dir:
+        type: str
+        default: static/images/
+        per_host: true
+        required: false
+        desc: |
+          Path to the static images directory. Ignored if static_enabled is false.
 
       static_favicon_dir:
         type: str
@@ -1908,10 +1909,8 @@ mapping:
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to favicon.ico, not the directory that contains it (the name is a
+          misnomer). Ignored if static_enabled is false.
 
       static_scripts_dir:
         type: str
@@ -1919,21 +1918,15 @@ mapping:
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to the static scripts directory. Ignored if static_enabled is false.
 
       static_style_dir:
         type: str
-        default: static/style
+        default: static/style/
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to the static style directory. Ignored if static_enabled is false.
 
       static_robots_txt:
         type: str
@@ -1941,10 +1934,7 @@ mapping:
         per_host: true
         required: false
         desc: |
-          Serve static content, which must be enabled if you're not serving it via a
-          proxy server.  These options should be self explanatory and so are not
-          documented individually.  You can use these paths (or ones in the proxy
-          server) to point to your own styles.
+          Path to robots.txt. Ignored if static_enabled is false.
 
       display_chunk_size:
         type: int
diff --git a/lib/galaxy/webapps/base/webapp.py b/lib/galaxy/webapps/base/webapp.py
index 58d967d63f6..f995c39054e 100644
--- a/lib/galaxy/webapps/base/webapp.py
+++ b/lib/galaxy/webapps/base/webapp.py
@@ -66,9 +66,9 @@ from galaxy.web.framework.middleware.static import CacheableStaticURLParser as S
 try:
     import galaxy.web_client
 
-    default_static_dir = os.path.dirname(galaxy.web_client.__file__)
+    default_static_dist_dir = os.path.join(os.path.dirname(galaxy.web_client.__file__), "dist")
 except ImportError:
-    default_static_dir = "static/"
+    default_static_dist_dir = None  # type: ignore[assignment]
 
 log = logging.getLogger(__name__)
 
@@ -1160,17 +1160,19 @@ def build_url_map(app, global_conf, **local_conf):
         return Static(config_val, cache_time, directory_per_host=per_host_config)
 
     # Define static mappings from config
-    static_dir = get_static_from_config("static_dir", default_static_dir)
+    static_dir = get_static_from_config("static_dir", "static/")
     static_dir_bare = static_dir.directory.rstrip("/")
+    static_dist_dir = get_static_from_config("static_dist_dir", default_static_dist_dir or f"{static_dir_bare}/dist/")
     urlmap["/static"] = static_dir
+    urlmap["/static/dist"] = static_dist_dir
     urlmap["/images"] = get_static_from_config("static_images_dir", f"{static_dir_bare}/images")
     urlmap["/static/scripts"] = get_static_from_config("static_scripts_dir", f"{static_dir_bare}/scripts/")
 
     urlmap["/static/welcome.html"] = get_static_from_config(
         "static_welcome_html", f"{static_dir_bare}/welcome.html", sample=default_url_path("static/welcome.sample.html")
     )
-    urlmap["/static/favicon.svg"] = get_static_from_config(
-        "static_favicon_dir", f"{static_dir_bare}/favicon.svg", sample=default_url_path("static/favicon.svg")
+    urlmap["/favicon.ico"] = get_static_from_config(
+        "static_favicon_dir", f"{static_dir_bare}/favicon.ico", sample=default_url_path("static/favicon.ico")
     )
     urlmap["/robots.txt"] = get_static_from_config(
         "static_robots_txt", f"{static_dir_bare}/robots.txt", sample=default_url_path("static/robots.txt")
diff --git a/packages/web_client/galaxy/web_client/install.py b/packages/web_client/galaxy/web_client/install.py
index f78cfeda8f7..09df111bc51 100644
--- a/packages/web_client/galaxy/web_client/install.py
+++ b/packages/web_client/galaxy/web_client/install.py
@@ -24,7 +24,24 @@ The --mode option specifies how the web client is installed:
         Copy the Galaxy web client to DEST
 """
 
-CLIENT = os.path.join(os.path.dirname(__file__))
+TARGETS = {
+    "dist": os.path.join(os.path.dirname(__file__), "dist"),
+}
+
+try:
+    import galaxy.webapps.base
+
+    STATIC = os.path.join(os.path.dirname(galaxy.webapps.base.__file__), "static")
+    TARGETS.update({
+        "style": os.path.join(STATIC, "style"),
+        "favicon.ico": os.path.join(STATIC, "favicon.ico"),
+        "favicon.svg": os.path.join(STATIC, "favicon.svg"),
+        "robots.txt": os.path.join(STATIC, "robots.txt"),
+        "welcome.sample.html": os.path.join(STATIC, "welcome.sample.html"),
+    })
+except ImportError:
+    # Consider this a soft fail, this package depends on nothing but is probably installed with galaxy-web-apps
+    pass
 
 
 def main(argv=None):
@@ -32,12 +49,15 @@ def main(argv=None):
         argv = sys.argv[1:]
     args = _arg_parser().parse_args(argv)
 
-    dist = os.path.join(CLIENT, "dist")
-    assert os.path.exists(dist), f"ERROR: Cannot find web client at expected path: {dist}"
-    if args.mode in ("absolute", "relative"):
-        _symlink(args.dest, args.mode == "absolute", args.force_overwrite)
-    elif args.mode == "copy":
-        _copy(args.dest, args.force_overwrite)
+    assert os.path.exists(TARGETS["dist"]), f"ERROR: Cannot find web client at expected path: {TARGETS['dist']}"
+
+    _try(functools.partial(os.makedirs, args.dest), args.dest, args.force_overwrite, dir_ok=True)
+    for dest, target in TARGETS.items():
+        dest = os.path.join(args.dest, dest)
+        if args.mode in ("absolute", "relative"):
+            _symlink(dest, target, args.mode == "absolute", args.force_overwrite)
+        elif args.mode == "copy":
+            _copy(dest, target, args.force_overwrite)
 
 
 def _arg_parser():
@@ -51,30 +71,47 @@ def _arg_parser():
     return parser
 
 
-def _symlink(dest, absolute, force):
+def _symlink(dest, target, absolute, force):
     if absolute:
-        target = os.path.abspath(CLIENT)
+        target = os.path.abspath(target)
     else:
-        target = os.path.relpath(CLIENT, start=dest)
-    _try(functools.partial(os.symlink, target, dest), dest, force)
+        target = os.path.relpath(target, start=os.path.dirname(dest))
+    if _try(functools.partial(os.symlink, target, dest), dest, force, target=target):
+        print(f"link: {dest} -> {target}")
 
 
-def _copy(dest, force):
-    _try(functools.partial(shutil.copytree, CLIENT, dest, dirs_exist_ok=False), dest, force)
+def _copy(dest, target, force):
+    if os.path.isdir(target):
+        f = functools.partial(shutil.copytree, target, dest, dirs_exist_ok=False)
+    else:
+        f = functools.partial(_copy2, target, dest)
+    if _try(f, dest, force):
+        print(f"copy: {target} -> {dest}")
 
 
-def _try(f, dest, force):
+def _copy2(target, dest):
+    if os.path.exists(dest):
+        raise FileExistsError(dest)
+    shutil.copy2(target, dest)
+
+
+def _try(f, dest, force, target=None, dir_ok=False):
     try:
         f()
-    except FileExistsError:
+    except (FileExistsError, shutil.SameFileError):
+        if dir_ok and os.path.isdir(dest) and not os.path.islink(dest):
+            return True
+        if target and os.path.islink(dest) and os.readlink(dest) == target:
+            return True
         if not force:
             print(f"ERROR: File exists, use --force-overwrite to overwrite: {dest}")
-            sys.exit(1)
+            return False
         if os.path.isdir(dest) and not os.path.islink(dest):
             shutil.rmtree(dest)
         else:
             os.unlink(dest)
         f()
+    return True
 
 
 if __name__ == "__main__":
diff --git a/packages/web_client/setup.cfg b/packages/web_client/setup.cfg
index e1e28f289bb..6410e454cd8 100644
--- a/packages/web_client/setup.cfg
+++ b/packages/web_client/setup.cfg
@@ -27,7 +27,7 @@ long_description = file: README.rst, HISTORY.rst
 long_description_content_type = text/x-rst
 name = galaxy-web-client
 url = https://github.com/galaxyproject/galaxy
-version = 25.0.dev0
+version = 25.0.1.dev0
 
 [options]
 include_package_data = True