diff --git a/src/Umbraco.Web.BackOffice/Services/IconService.cs b/src/Umbraco.Web.BackOffice/Services/IconService.cs
index 7f060dc756..c8b6eaaf1b 100644
--- a/src/Umbraco.Web.BackOffice/Services/IconService.cs
+++ b/src/Umbraco.Web.BackOffice/Services/IconService.cs
@@ -136,6 +136,9 @@ public class IconService : IIconService
             }
         }
 
+        // Get icons from the web root file provider (both physical and virtual)
+        icons.UnionWith(GetIconsFiles(_webHostEnvironment.WebRootFileProvider, Constants.SystemDirectories.AppPlugins));
+
         IDirectoryContents? iconFolder =
             _webHostEnvironment.WebRootFileProvider.GetDirectoryContents(_globalSettings.IconsPath);
 
@@ -148,6 +151,63 @@ public class IconService : IIconService
         return icons;
     }
 
+
+    /// <summary>
+    /// Finds all SVG icon files based on the specified <paramref name="fileProvider"/> and <paramref name="path"/>.
+    /// The method will find both physical and virtual (eg. from a Razor Class Library) icons.
+    /// </summary>
+    /// <param name="fileProvider">The file provider to be used.</param>
+    /// <param name="path">The sub path to start from - should probably always be <see cref="Constants.SystemDirectories.AppPlugins"/>.</param>
+    /// <returns>A collection of <see cref="FileInfo"/> representing the found SVG icon files.</returns>
+    private static IEnumerable<FileInfo> GetIconsFiles(IFileProvider fileProvider, string path)
+    {
+        // Iterate through all plugin folders, this is necessary because on Linux we'll get casing issues when
+        // we directly try to access {path}/{pluginDirectory.Name}/{Constants.SystemDirectories.PluginIcons}
+        foreach (IFileInfo pluginDirectory in fileProvider.GetDirectoryContents(path))
+        {
+            // Ideally there shouldn't be any files, but we'd better check to be sure
+            if (!pluginDirectory.IsDirectory)
+            {
+                continue;
+            }
+
+            // Iterate through the sub directories of each plugin folder
+            foreach (IFileInfo subDir1 in fileProvider.GetDirectoryContents($"{path}/{pluginDirectory.Name}"))
+            {
+                // Skip files again
+                if (!subDir1.IsDirectory)
+                {
+                    continue;
+                }
+
+                // Iterate through second level sub directories
+                foreach (IFileInfo subDir2 in fileProvider.GetDirectoryContents($"{path}/{pluginDirectory.Name}/{subDir1.Name}"))
+                {
+                    // Skip files again
+                    if (!subDir2.IsDirectory)
+                    {
+                        continue;
+                    }
+
+                    // Does the directory match the plugin icons folder? (case insensitive for legacy support)
+                    if (!$"/{subDir1.Name}/{subDir2.Name}".InvariantEquals(Constants.SystemDirectories.PluginIcons))
+                    {
+                        continue;
+                    }
+
+                    // Iterate though the files of the second level sub directory. This should be where the SVG files are located :D
+                    foreach (IFileInfo file in fileProvider.GetDirectoryContents($"{path}/{pluginDirectory.Name}/{subDir1.Name}/{subDir2.Name}"))
+                    {
+                        if (file.Name.InvariantEndsWith(".svg"))
+                        {
+                            yield return new FileInfo(file.PhysicalPath);
+                        }
+                    }
+                }
+            }
+        }
+    }
+
     private IReadOnlyDictionary<string, string>? GetIconDictionary() => _cache.GetCacheItem(
         $"{typeof(IconService).FullName}.{nameof(GetIconDictionary)}",
         () => GetAllIconsFiles()