diff --git a/Emby.Server.Implementations/Library/PathExtensions.cs b/Emby.Server.Implementations/Library/PathExtensions.cs
index 64e7d54466..c4b6b37561 100644
--- a/Emby.Server.Implementations/Library/PathExtensions.cs
+++ b/Emby.Server.Implementations/Library/PathExtensions.cs
@@ -1,5 +1,6 @@
 using System;
 using System.Diagnostics.CodeAnalysis;
+using System.IO;
 using MediaBrowser.Common.Providers;
 
 namespace Emby.Server.Implementations.Library
@@ -86,24 +87,8 @@ namespace Emby.Server.Implementations.Library
                 return false;
             }
 
-            char oldDirectorySeparatorChar;
-            char newDirectorySeparatorChar;
-            // True normalization is still not possible https://github.com/dotnet/runtime/issues/2162
-            // The reasoning behind this is that a forward slash likely means it's a Linux path and
-            // so the whole path should be normalized to use / and vice versa for Windows (although Windows doesn't care much).
-            if (newSubPath.Contains('/', StringComparison.Ordinal))
-            {
-                oldDirectorySeparatorChar = '\\';
-                newDirectorySeparatorChar = '/';
-            }
-            else
-            {
-                oldDirectorySeparatorChar = '/';
-                newDirectorySeparatorChar = '\\';
-            }
-
-            path = path.Replace(oldDirectorySeparatorChar, newDirectorySeparatorChar);
-            subPath = subPath.Replace(oldDirectorySeparatorChar, newDirectorySeparatorChar);
+            subPath = subPath.NormalizePath(out var newDirectorySeparatorChar);
+            path = path.NormalizePath(newDirectorySeparatorChar);
 
             // We have to ensure that the sub path ends with a directory separator otherwise we'll get weird results
             // when the sub path matches a similar but in-complete subpath
@@ -127,5 +112,82 @@ namespace Emby.Server.Implementations.Library
 
             return true;
         }
+
+        /// <summary>
+        /// Retrieves the full resolved path and normalizes path separators to the <see cref="Path.DirectorySeparatorChar"/>.
+        /// </summary>
+        /// <param name="path">The path to canonicalize.</param>
+        /// <returns>The fully expanded, normalized path.</returns>
+        public static string Canonicalize(this string path)
+        {
+            return Path.GetFullPath(path).NormalizePath();
+        }
+
+        /// <summary>
+        /// Normalizes the path's directory separator character to the currently defined <see cref="Path.DirectorySeparatorChar"/>.
+        /// </summary>
+        /// <param name="path">The path to normalize.</param>
+        /// <returns>The normalized path string or <see langword="null"/> if the input path is null or empty.</returns>
+        [return: NotNullIfNotNull(nameof(path))]
+        public static string? NormalizePath(this string? path)
+        {
+            return path.NormalizePath(Path.DirectorySeparatorChar);
+        }
+
+        /// <summary>
+        /// Normalizes the path's directory separator character.
+        /// </summary>
+        /// <param name="path">The path to normalize.</param>
+        /// <param name="separator">The separator character the path now uses or <see langword="null"/>.</param>
+        /// <returns>The normalized path string or <see langword="null"/> if the input path is null or empty.</returns>
+        [return: NotNullIfNotNull(nameof(path))]
+        public static string? NormalizePath(this string? path, out char separator)
+        {
+            if (string.IsNullOrEmpty(path))
+            {
+                separator = default;
+                return path;
+            }
+
+            var newSeparator = '\\';
+
+            // True normalization is still not possible https://github.com/dotnet/runtime/issues/2162
+            // The reasoning behind this is that a forward slash likely means it's a Linux path and
+            // so the whole path should be normalized to use / and vice versa for Windows (although Windows doesn't care much).
+            if (path.Contains('/', StringComparison.Ordinal))
+            {
+                newSeparator = '/';
+            }
+
+            separator = newSeparator;
+
+            return path.NormalizePath(newSeparator);
+        }
+
+        /// <summary>
+        /// Normalizes the path's directory separator character to the specified character.
+        /// </summary>
+        /// <param name="path">The path to normalize.</param>
+        /// <param name="newSeparator">The replacement directory separator character. Must be a valid directory separator.</param>
+        /// <returns>The normalized path.</returns>
+        /// <exception cref="ArgumentException">Thrown if the new separator character is not a directory separator.</exception>
+        [return: NotNullIfNotNull(nameof(path))]
+        public static string? NormalizePath(this string? path, char newSeparator)
+        {
+            const char Bs = '\\';
+            const char Fs = '/';
+
+            if (!(newSeparator == Bs || newSeparator == Fs))
+            {
+                throw new ArgumentException("The character must be a directory separator.");
+            }
+
+            if (string.IsNullOrEmpty(path))
+            {
+                return path;
+            }
+
+            return newSeparator == Bs ? path.Replace(Fs, newSeparator) : path.Replace(Bs, newSeparator);
+        }
     }
 }
diff --git a/Emby.Server.Implementations/Plugins/PluginManager.cs b/Emby.Server.Implementations/Plugins/PluginManager.cs
index f14f87ccda..48584ae0cb 100644
--- a/Emby.Server.Implementations/Plugins/PluginManager.cs
+++ b/Emby.Server.Implementations/Plugins/PluginManager.cs
@@ -1,5 +1,6 @@
 using System;
 using System.Collections.Generic;
+using System.Data;
 using System.Globalization;
 using System.IO;
 using System.Linq;
@@ -9,6 +10,8 @@ using System.Runtime.Loader;
 using System.Text;
 using System.Text.Json;
 using System.Threading.Tasks;
+using Emby.Server.Implementations.Library;
+using Jellyfin.Extensions;
 using Jellyfin.Extensions.Json;
 using Jellyfin.Extensions.Json.Converters;
 using MediaBrowser.Common;
@@ -29,6 +32,8 @@ namespace Emby.Server.Implementations.Plugins
     /// </summary>
     public class PluginManager : IPluginManager
     {
+        private const string MetafileName = "meta.json";
+
         private readonly string _pluginsPath;
         private readonly Version _appVersion;
         private readonly List<AssemblyLoadContext> _assemblyLoadContexts;
@@ -44,7 +49,7 @@ namespace Emby.Server.Implementations.Plugins
         /// <summary>
         /// Initializes a new instance of the <see cref="PluginManager"/> class.
         /// </summary>
-        /// <param name="logger">The <see cref="ILogger"/>.</param>
+        /// <param name="logger">The <see cref="ILogger{PluginManager}"/>.</param>
         /// <param name="appHost">The <see cref="IApplicationHost"/>.</param>
         /// <param name="config">The <see cref="ServerConfiguration"/>.</param>
         /// <param name="pluginsPath">The plugin path.</param>
@@ -371,7 +376,7 @@ namespace Emby.Server.Implementations.Plugins
             try
             {
                 var data = JsonSerializer.Serialize(manifest, _jsonOptions);
-                File.WriteAllText(Path.Combine(path, "meta.json"), data);
+                File.WriteAllText(Path.Combine(path, MetafileName), data);
                 return true;
             }
             catch (ArgumentException e)
@@ -382,7 +387,7 @@ namespace Emby.Server.Implementations.Plugins
         }
 
         /// <inheritdoc/>
-        public async Task<bool> GenerateManifest(PackageInfo packageInfo, Version version, string path, PluginStatus status)
+        public async Task<bool> PopulateManifest(PackageInfo packageInfo, Version version, string path, PluginStatus status)
         {
             var versionInfo = packageInfo.Versions.First(v => v.Version == version.ToString());
             var imagePath = string.Empty;
@@ -427,9 +432,71 @@ namespace Emby.Server.Implementations.Plugins
                 ImagePath = imagePath
             };
 
+            if (!await ReconcileManifest(manifest, path))
+            {
+                // An error occurred during reconciliation and saving could be undesirable.
+                return false;
+            }
+
             return SaveManifest(manifest, path);
         }
 
+        /// <summary>
+        /// Reconciles the manifest against any properties that exist locally in a pre-packaged meta.json found at the path.
+        /// If no file is found, no reconciliation occurs.
+        /// </summary>
+        /// <param name="manifest">The <see cref="PluginManifest"/> to reconcile against.</param>
+        /// <param name="path">The plugin path.</param>
+        /// <returns>The reconciled <see cref="PluginManifest"/>.</returns>
+        private async Task<bool> ReconcileManifest(PluginManifest manifest, string path)
+        {
+            try
+            {
+                var metafile = Path.Combine(path, MetafileName);
+                if (!File.Exists(metafile))
+                {
+                    _logger.LogInformation("No local manifest exists for plugin {Plugin}. Skipping manifest reconciliation.", manifest.Name);
+                    return true;
+                }
+
+                using var metaStream = File.OpenRead(metafile);
+                var localManifest = await JsonSerializer.DeserializeAsync<PluginManifest>(metaStream, _jsonOptions);
+                localManifest ??= new PluginManifest();
+
+                if (!Equals(localManifest.Id, manifest.Id))
+                {
+                    _logger.LogError("The manifest ID {LocalUUID} did not match the package info ID {PackageUUID}.", localManifest.Id, manifest.Id);
+                    manifest.Status = PluginStatus.Malfunctioned;
+                }
+
+                if (localManifest.Version != manifest.Version)
+                {
+                    // Package information provides the version and is the source of truth. Pre-packages meta.json is assumed to be a mistake in this regard.
+                    _logger.LogWarning("The version of the local manifest was {LocalVersion}, but {PackageVersion} was expected. The value will be replaced.", localManifest.Version, manifest.Version);
+                }
+
+                // Explicitly mapping properties instead of using reflection is preferred here.
+                manifest.Category = string.IsNullOrEmpty(localManifest.Category) ? manifest.Category : localManifest.Category;
+                manifest.AutoUpdate = localManifest.AutoUpdate; // Preserve whatever is local. Package info does not have this property.
+                manifest.Changelog = string.IsNullOrEmpty(localManifest.Changelog) ? manifest.Changelog : localManifest.Changelog;
+                manifest.Description = string.IsNullOrEmpty(localManifest.Description) ? manifest.Description : localManifest.Description;
+                manifest.Name = string.IsNullOrEmpty(localManifest.Name) ? manifest.Name : localManifest.Name;
+                manifest.Overview = string.IsNullOrEmpty(localManifest.Overview) ? manifest.Overview : localManifest.Overview;
+                manifest.Owner = string.IsNullOrEmpty(localManifest.Owner) ? manifest.Owner : localManifest.Owner;
+                manifest.TargetAbi = string.IsNullOrEmpty(localManifest.TargetAbi) ? manifest.TargetAbi : localManifest.TargetAbi;
+                manifest.Timestamp = localManifest.Timestamp.Equals(default) ? manifest.Timestamp : localManifest.Timestamp;
+                manifest.ImagePath = string.IsNullOrEmpty(localManifest.ImagePath) ? manifest.ImagePath : localManifest.ImagePath;
+                manifest.Assemblies = localManifest.Assemblies;
+
+                return true;
+            }
+            catch (Exception e)
+            {
+                _logger.LogWarning(e, "Unable to reconcile plugin manifest due to an error. {Path}", path);
+                return false;
+            }
+        }
+
         /// <summary>
         /// Changes a plugin's load status.
         /// </summary>
@@ -594,7 +661,7 @@ namespace Emby.Server.Implementations.Plugins
         {
             Version? version;
             PluginManifest? manifest = null;
-            var metafile = Path.Combine(dir, "meta.json");
+            var metafile = Path.Combine(dir, MetafileName);
             if (File.Exists(metafile))
             {
                 // Only path where this stays null is when File.ReadAllBytes throws an IOException
@@ -688,7 +755,15 @@ namespace Emby.Server.Implementations.Plugins
                 var entry = versions[x];
                 if (!string.Equals(lastName, entry.Name, StringComparison.OrdinalIgnoreCase))
                 {
-                    entry.DllFiles = Directory.GetFiles(entry.Path, "*.dll", SearchOption.AllDirectories);
+                    if (!TryGetPluginDlls(entry, out var allowedDlls))
+                    {
+                        _logger.LogError("One or more assembly paths was invalid. Marking plugin {Plugin} as \"Malfunctioned\".", entry.Name);
+                        ChangePluginState(entry, PluginStatus.Malfunctioned);
+                        continue;
+                    }
+
+                    entry.DllFiles = allowedDlls;
+
                     if (entry.IsEnabledAndSupported)
                     {
                         lastName = entry.Name;
@@ -734,6 +809,68 @@ namespace Emby.Server.Implementations.Plugins
             return versions.Where(p => p.DllFiles.Count != 0);
         }
 
+        /// <summary>
+        /// Attempts to retrieve valid DLLs from the plugin path. This method will consider the assembly whitelist
+        /// from the manifest.
+        /// </summary>
+        /// <remarks>
+        /// Loading DLLs from externally supplied paths introduces a path traversal risk. This method
+        /// uses a safelisting tactic of considering DLLs from the plugin directory and only using
+        /// the plugin's canonicalized assembly whitelist for comparison. See
+        /// <see href="https://owasp.org/www-community/attacks/Path_Traversal"/> for more details.
+        /// </remarks>
+        /// <param name="plugin">The plugin.</param>
+        /// <param name="whitelistedDlls">The whitelisted DLLs. If the method returns <see langword="false"/>, this will be empty.</param>
+        /// <returns>
+        /// <see langword="true"/> if all assemblies listed in the manifest were available in the plugin directory.
+        /// <see langword="false"/> if any assemblies were invalid or missing from the plugin directory.
+        /// </returns>
+        /// <exception cref="ArgumentNullException">If the <see cref="LocalPlugin"/> is null.</exception>
+        private bool TryGetPluginDlls(LocalPlugin plugin, out IReadOnlyList<string> whitelistedDlls)
+        {
+            ArgumentNullException.ThrowIfNull(nameof(plugin));
+
+            IReadOnlyList<string> pluginDlls = Directory.GetFiles(plugin.Path, "*.dll", SearchOption.AllDirectories);
+
+            whitelistedDlls = Array.Empty<string>();
+            if (pluginDlls.Count > 0 && plugin.Manifest.Assemblies.Count > 0)
+            {
+                _logger.LogInformation("Registering whitelisted assemblies for plugin \"{Plugin}\"...", plugin.Name);
+
+                var canonicalizedPaths = new List<string>();
+                foreach (var path in plugin.Manifest.Assemblies)
+                {
+                    var canonicalized = Path.Combine(plugin.Path, path).Canonicalize();
+
+                    // Ensure we stay in the plugin directory.
+                    if (!canonicalized.StartsWith(plugin.Path.NormalizePath(), StringComparison.Ordinal))
+                    {
+                        _logger.LogError("Assembly path {Path} is not inside the plugin directory.", path);
+                        return false;
+                    }
+
+                    canonicalizedPaths.Add(canonicalized);
+                }
+
+                var intersected = pluginDlls.Intersect(canonicalizedPaths).ToList();
+
+                if (intersected.Count != canonicalizedPaths.Count)
+                {
+                    _logger.LogError("Plugin {Plugin} contained assembly paths that were not found in the directory.", plugin.Name);
+                    return false;
+                }
+
+                whitelistedDlls = intersected;
+            }
+            else
+            {
+                // No whitelist, default to loading all DLLs in plugin directory.
+                whitelistedDlls = pluginDlls;
+            }
+
+            return true;
+        }
+
         /// <summary>
         /// Changes the status of the other versions of the plugin to "Superceded".
         /// </summary>
diff --git a/Emby.Server.Implementations/Updates/InstallationManager.cs b/Emby.Server.Implementations/Updates/InstallationManager.cs
index 5e897833e0..6c198b6f99 100644
--- a/Emby.Server.Implementations/Updates/InstallationManager.cs
+++ b/Emby.Server.Implementations/Updates/InstallationManager.cs
@@ -183,7 +183,7 @@ namespace Emby.Server.Implementations.Updates
                             var plugin = _pluginManager.GetPlugin(package.Id, version.VersionNumber);
                             if (plugin is not null)
                             {
-                                await _pluginManager.GenerateManifest(package, version.VersionNumber, plugin.Path, plugin.Manifest.Status).ConfigureAwait(false);
+                                await _pluginManager.PopulateManifest(package, version.VersionNumber, plugin.Path, plugin.Manifest.Status).ConfigureAwait(false);
                             }
 
                             // Remove versions with a target ABI greater then the current application version.
@@ -555,7 +555,10 @@ namespace Emby.Server.Implementations.Updates
             stream.Position = 0;
             using var reader = new ZipArchive(stream);
             reader.ExtractToDirectory(targetDir, true);
-            await _pluginManager.GenerateManifest(package.PackageInfo, package.Version, targetDir, status).ConfigureAwait(false);
+
+            // Ensure we create one or populate existing ones with missing data.
+            await _pluginManager.PopulateManifest(package.PackageInfo, package.Version, targetDir, status);
+
             _pluginManager.ImportPluginFrom(targetDir);
         }
 
diff --git a/MediaBrowser.Common/Plugins/IPluginManager.cs b/MediaBrowser.Common/Plugins/IPluginManager.cs
index fa92d383a2..1d73de3c95 100644
--- a/MediaBrowser.Common/Plugins/IPluginManager.cs
+++ b/MediaBrowser.Common/Plugins/IPluginManager.cs
@@ -57,7 +57,7 @@ namespace MediaBrowser.Common.Plugins
         /// <param name="path">The path where to save the manifest.</param>
         /// <param name="status">Initial status of the plugin.</param>
         /// <returns>True if successful.</returns>
-        Task<bool> GenerateManifest(PackageInfo packageInfo, Version version, string path, PluginStatus status);
+        Task<bool> PopulateManifest(PackageInfo packageInfo, Version version, string path, PluginStatus status);
 
         /// <summary>
         /// Imports plugin details from a folder.
diff --git a/MediaBrowser.Common/Plugins/PluginManifest.cs b/MediaBrowser.Common/Plugins/PluginManifest.cs
index 2910dbe144..e0847ccea4 100644
--- a/MediaBrowser.Common/Plugins/PluginManifest.cs
+++ b/MediaBrowser.Common/Plugins/PluginManifest.cs
@@ -1,4 +1,5 @@
 using System;
+using System.Collections.Generic;
 using System.Text.Json.Serialization;
 using MediaBrowser.Model.Plugins;
 
@@ -23,6 +24,7 @@ namespace MediaBrowser.Common.Plugins
             Overview = string.Empty;
             TargetAbi = string.Empty;
             Version = string.Empty;
+            Assemblies = Array.Empty<string>();
         }
 
         /// <summary>
@@ -104,5 +106,12 @@ namespace MediaBrowser.Common.Plugins
         /// </summary>
         [JsonPropertyName("imagePath")]
         public string? ImagePath { get; set; }
+
+        /// <summary>
+        /// Gets or sets the collection of assemblies that should be loaded.
+        /// Paths are considered relative to the plugin folder.
+        /// </summary>
+        [JsonPropertyName("assemblies")]
+        public IReadOnlyList<string> Assemblies { get; set; }
     }
 }
diff --git a/tests/Jellyfin.Server.Implementations.Tests/Library/PathExtensionsTests.cs b/tests/Jellyfin.Server.Implementations.Tests/Library/PathExtensionsTests.cs
index be2dfe0a86..c33a957e69 100644
--- a/tests/Jellyfin.Server.Implementations.Tests/Library/PathExtensionsTests.cs
+++ b/tests/Jellyfin.Server.Implementations.Tests/Library/PathExtensionsTests.cs
@@ -1,4 +1,5 @@
 using System;
+using System.IO;
 using Emby.Server.Implementations.Library;
 using Xunit;
 
@@ -73,5 +74,47 @@ namespace Jellyfin.Server.Implementations.Tests.Library
             Assert.False(PathExtensions.TryReplaceSubPath(path, subPath, newSubPath, out var result));
             Assert.Null(result);
         }
+
+        [Theory]
+        [InlineData(null, '/', null)]
+        [InlineData(null, '\\', null)]
+        [InlineData("/home/jeff/myfile.mkv", '\\', "\\home\\jeff\\myfile.mkv")]
+        [InlineData("C:\\Users\\Jeff\\myfile.mkv", '/', "C:/Users/Jeff/myfile.mkv")]
+        [InlineData("\\home/jeff\\myfile.mkv", '\\', "\\home\\jeff\\myfile.mkv")]
+        [InlineData("\\home/jeff\\myfile.mkv", '/', "/home/jeff/myfile.mkv")]
+        [InlineData("", '/', "")]
+        public void NormalizePath_SpecifyingSeparator_Normalizes(string path, char separator, string expectedPath)
+        {
+            Assert.Equal(expectedPath, path.NormalizePath(separator));
+        }
+
+        [Theory]
+        [InlineData("/home/jeff/myfile.mkv")]
+        [InlineData("C:\\Users\\Jeff\\myfile.mkv")]
+        [InlineData("\\home/jeff\\myfile.mkv")]
+        public void NormalizePath_NoArgs_UsesDirectorySeparatorChar(string path)
+        {
+            var separator = Path.DirectorySeparatorChar;
+
+            Assert.Equal(path.Replace('\\', separator).Replace('/', separator), path.NormalizePath());
+        }
+
+        [Theory]
+        [InlineData("/home/jeff/myfile.mkv", '/')]
+        [InlineData("C:\\Users\\Jeff\\myfile.mkv", '\\')]
+        [InlineData("\\home/jeff\\myfile.mkv", '/')]
+        public void NormalizePath_OutVar_Correct(string path, char expectedSeparator)
+        {
+            var result = path.NormalizePath(out var separator);
+
+            Assert.Equal(expectedSeparator, separator);
+            Assert.Equal(path.Replace('\\', separator).Replace('/', separator), result);
+        }
+
+        [Fact]
+        public void NormalizePath_SpecifyInvalidSeparator_ThrowsException()
+        {
+            Assert.Throws<ArgumentException>(() => string.Empty.NormalizePath('a'));
+        }
     }
 }
diff --git a/tests/Jellyfin.Server.Implementations.Tests/Plugins/PluginManagerTests.cs b/tests/Jellyfin.Server.Implementations.Tests/Plugins/PluginManagerTests.cs
index bc6a447410..d4b90dac02 100644
--- a/tests/Jellyfin.Server.Implementations.Tests/Plugins/PluginManagerTests.cs
+++ b/tests/Jellyfin.Server.Implementations.Tests/Plugins/PluginManagerTests.cs
@@ -1,7 +1,16 @@
 using System;
+using System.Globalization;
 using System.IO;
+using System.Text.Json;
+using System.Threading.Tasks;
+using AutoFixture;
+using Emby.Server.Implementations.Library;
 using Emby.Server.Implementations.Plugins;
+using Jellyfin.Extensions.Json;
+using Jellyfin.Extensions.Json.Converters;
 using MediaBrowser.Common.Plugins;
+using MediaBrowser.Model.Plugins;
+using MediaBrowser.Model.Updates;
 using Microsoft.Extensions.Logging.Abstractions;
 using Xunit;
 
@@ -11,6 +20,21 @@ namespace Jellyfin.Server.Implementations.Tests.Plugins
     {
         private static readonly string _testPathRoot = Path.Combine(Path.GetTempPath(), "jellyfin-test-data");
 
+        private string _tempPath = string.Empty;
+
+        private string _pluginPath = string.Empty;
+
+        private JsonSerializerOptions _options;
+
+        public PluginManagerTests()
+        {
+            (_tempPath, _pluginPath) = GetTestPaths("plugin-" + Path.GetRandomFileName());
+
+            Directory.CreateDirectory(_pluginPath);
+
+            _options = GetTestSerializerOptions();
+        }
+
         [Fact]
         public void SaveManifest_RoundTrip_Success()
         {
@@ -20,12 +44,9 @@ namespace Jellyfin.Server.Implementations.Tests.Plugins
                 Version = "1.0"
             };
 
-            var tempPath = Path.Combine(_testPathRoot, "manifest-" + Path.GetRandomFileName());
-            Directory.CreateDirectory(tempPath);
+            Assert.True(pluginManager.SaveManifest(manifest, _pluginPath));
 
-            Assert.True(pluginManager.SaveManifest(manifest, tempPath));
-
-            var res = pluginManager.LoadManifest(tempPath);
+            var res = pluginManager.LoadManifest(_pluginPath);
 
             Assert.Equal(manifest.Category, res.Manifest.Category);
             Assert.Equal(manifest.Changelog, res.Manifest.Changelog);
@@ -40,6 +61,278 @@ namespace Jellyfin.Server.Implementations.Tests.Plugins
             Assert.Equal(manifest.Status, res.Manifest.Status);
             Assert.Equal(manifest.AutoUpdate, res.Manifest.AutoUpdate);
             Assert.Equal(manifest.ImagePath, res.Manifest.ImagePath);
+            Assert.Equal(manifest.Assemblies, res.Manifest.Assemblies);
+        }
+
+        /// <summary>
+        ///  Tests safe traversal within the plugin directory.
+        /// </summary>
+        /// <param name="dllFile">The safe path to evaluate.</param>
+        [Theory]
+        [InlineData("./some.dll")]
+        [InlineData("some.dll")]
+        [InlineData("sub/path/some.dll")]
+        public void Constructor_DiscoversSafePluginAssembly_Status_Active(string dllFile)
+        {
+            var manifest = new PluginManifest
+            {
+                Id = Guid.NewGuid(),
+                Name = "Safe Assembly",
+                Assemblies = new string[] { dllFile }
+            };
+
+            var filename = Path.GetFileName(dllFile)!;
+            var dllPath = Path.GetDirectoryName(Path.Combine(_pluginPath, dllFile))!;
+
+            Directory.CreateDirectory(dllPath);
+            File.Create(Path.Combine(dllPath, filename));
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+
+            File.WriteAllText(metafilePath, JsonSerializer.Serialize(manifest, _options));
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, _tempPath, new Version(1, 0));
+
+            var res = JsonSerializer.Deserialize<PluginManifest>(File.ReadAllText(metafilePath), _options);
+
+            var expectedFullPath = Path.Combine(_pluginPath, dllFile).Canonicalize();
+
+            Assert.NotNull(res);
+            Assert.NotEmpty(pluginManager.Plugins);
+            Assert.Equal(PluginStatus.Active, res!.Status);
+            Assert.Equal(expectedFullPath, pluginManager.Plugins[0].DllFiles[0]);
+            Assert.StartsWith(_pluginPath, expectedFullPath, StringComparison.InvariantCulture);
+        }
+
+        /// <summary>
+        ///  Tests unsafe attempts to traverse to higher directories.
+        /// </summary>
+        /// <remarks>
+        ///  Attempts to load directories outside of the plugin should be
+        ///  constrained. Path traversal, shell expansion, and double encoding
+        ///  can be used to load unintended files.
+        ///  See <see href="https://owasp.org/www-community/attacks/Path_Traversal"/> for more.
+        /// </remarks>
+        /// <param name="unsafePath">The unsafe path to evaluate.</param>
+        [Theory]
+        [InlineData("/some.dll")] // Root path.
+        [InlineData("../some.dll")] // Simple traversal.
+        [InlineData("C:\\some.dll")] // Windows root path.
+        [InlineData("test.txt")] // Not a DLL
+        [InlineData(".././.././../some.dll")] // Traversal with current and parent
+        [InlineData("..\\.\\..\\.\\..\\some.dll")] // Windows traversal with current and parent
+        [InlineData("\\\\network\\resource.dll")] // UNC Path
+        [InlineData("https://jellyfin.org/some.dll")] // URL
+        [InlineData("~/some.dll")] // Tilde poses a shell expansion risk, but is a valid path character.
+        public void Constructor_DiscoversUnsafePluginAssembly_Status_Malfunctioned(string unsafePath)
+        {
+            var manifest = new PluginManifest
+            {
+                Id = Guid.NewGuid(),
+                Name = "Unsafe Assembly",
+                Assemblies = new string[] { unsafePath }
+            };
+
+            // Only create very specific files. Otherwise the test will be exploiting path traversal.
+            var files = new string[]
+            {
+                "../other.dll",
+                "some.dll"
+            };
+
+            foreach (var file in files)
+            {
+                File.Create(Path.Combine(_pluginPath, file));
+            }
+
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+
+            File.WriteAllText(metafilePath, JsonSerializer.Serialize(manifest, _options));
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, _tempPath, new Version(1, 0));
+
+            var res = JsonSerializer.Deserialize<PluginManifest>(File.ReadAllText(metafilePath), _options);
+
+            Assert.NotNull(res);
+            Assert.Empty(pluginManager.Plugins);
+            Assert.Equal(PluginStatus.Malfunctioned, res!.Status);
+        }
+
+        [Fact]
+        public async Task PopulateManifest_ExistingMetafilePlugin_PopulatesMissingFields()
+        {
+            var packageInfo = GenerateTestPackage();
+
+            // Partial plugin without a name, but matching version and package ID
+            var partial = new PluginManifest
+            {
+                Id = packageInfo.Id,
+                AutoUpdate = false, // Turn off AutoUpdate
+                Status = PluginStatus.Restart,
+                Version = new Version(1, 0, 0).ToString(),
+                Assemblies = new[] { "Jellyfin.Test.dll" }
+            };
+
+            var expectedManifest = new PluginManifest
+            {
+                Id = partial.Id,
+                Name = packageInfo.Name,
+                AutoUpdate = partial.AutoUpdate,
+                Status = PluginStatus.Active,
+                Owner = packageInfo.Owner,
+                Assemblies = partial.Assemblies,
+                Category = packageInfo.Category,
+                Description = packageInfo.Description,
+                Overview = packageInfo.Overview,
+                TargetAbi = packageInfo.Versions[0].TargetAbi!,
+                Timestamp = DateTime.Parse(packageInfo.Versions[0].Timestamp!, CultureInfo.InvariantCulture),
+                Changelog = packageInfo.Versions[0].Changelog!,
+                Version = new Version(1, 0).ToString(),
+                ImagePath = string.Empty
+            };
+
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+            File.WriteAllText(metafilePath, JsonSerializer.Serialize(partial, _options));
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, _tempPath, new Version(1, 0));
+
+            await pluginManager.PopulateManifest(packageInfo, new Version(1, 0), _pluginPath, PluginStatus.Active);
+
+            var resultBytes = File.ReadAllBytes(metafilePath);
+            var result = JsonSerializer.Deserialize<PluginManifest>(resultBytes, _options);
+
+            Assert.NotNull(result);
+            Assert.Equivalent(expectedManifest, result);
+        }
+
+        [Fact]
+        public async Task PopulateManifest_NoMetafile_PreservesManifest()
+        {
+            var packageInfo = GenerateTestPackage();
+            var expectedManifest = new PluginManifest
+            {
+                Id = packageInfo.Id,
+                Name = packageInfo.Name,
+                AutoUpdate = true,
+                Status = PluginStatus.Active,
+                Owner = packageInfo.Owner,
+                Assemblies = Array.Empty<string>(),
+                Category = packageInfo.Category,
+                Description = packageInfo.Description,
+                Overview = packageInfo.Overview,
+                TargetAbi = packageInfo.Versions[0].TargetAbi!,
+                Timestamp = DateTime.Parse(packageInfo.Versions[0].Timestamp!, CultureInfo.InvariantCulture),
+                Changelog = packageInfo.Versions[0].Changelog!,
+                Version = packageInfo.Versions[0].Version,
+                ImagePath = string.Empty
+            };
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, null!, new Version(1, 0));
+
+            await pluginManager.PopulateManifest(packageInfo, new Version(1, 0), _pluginPath, PluginStatus.Active);
+
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+            var resultBytes = File.ReadAllBytes(metafilePath);
+            var result = JsonSerializer.Deserialize<PluginManifest>(resultBytes, _options);
+
+            Assert.NotNull(result);
+            Assert.Equivalent(expectedManifest, result);
+        }
+
+        [Fact]
+        public async Task PopulateManifest_ExistingMetafileMismatchedIds_Status_Malfunctioned()
+        {
+            var packageInfo = GenerateTestPackage();
+
+            // Partial plugin without a name, but matching version and package ID
+            var partial = new PluginManifest
+            {
+                Id = Guid.NewGuid(),
+                Version = new Version(1, 0, 0).ToString()
+            };
+
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+            File.WriteAllText(metafilePath, JsonSerializer.Serialize(partial, _options));
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, _tempPath, new Version(1, 0));
+
+            await pluginManager.PopulateManifest(packageInfo, new Version(1, 0), _pluginPath, PluginStatus.Active);
+
+            var resultBytes = File.ReadAllBytes(metafilePath);
+            var result = JsonSerializer.Deserialize<PluginManifest>(resultBytes, _options);
+
+            Assert.NotNull(result);
+            Assert.Equal(packageInfo.Name, result.Name);
+            Assert.Equal(PluginStatus.Malfunctioned, result.Status);
+        }
+
+        [Fact]
+        public async Task PopulateManifest_ExistingMetafileMismatchedVersions_Updates_Version()
+        {
+            var packageInfo = GenerateTestPackage();
+
+            var partial = new PluginManifest
+            {
+                Id = packageInfo.Id,
+                Version = new Version(2, 0, 0).ToString()
+            };
+
+            var metafilePath = Path.Combine(_pluginPath, "meta.json");
+            File.WriteAllText(metafilePath, JsonSerializer.Serialize(partial, _options));
+
+            var pluginManager = new PluginManager(new NullLogger<PluginManager>(), null!, null!, _tempPath, new Version(1, 0));
+
+            await pluginManager.PopulateManifest(packageInfo, new Version(1, 0), _pluginPath, PluginStatus.Active);
+
+            var resultBytes = File.ReadAllBytes(metafilePath);
+            var result = JsonSerializer.Deserialize<PluginManifest>(resultBytes, _options);
+
+            Assert.NotNull(result);
+            Assert.Equal(packageInfo.Name, result.Name);
+            Assert.Equal(PluginStatus.Active, result.Status);
+            Assert.Equal(packageInfo.Versions[0].Version, result.Version);
+        }
+
+        private PackageInfo GenerateTestPackage()
+        {
+            var fixture = new Fixture();
+            fixture.Customize<PackageInfo>(c => c.Without(x => x.Versions).Without(x => x.ImageUrl));
+            fixture.Customize<VersionInfo>(c => c.Without(x => x.Version).Without(x => x.Timestamp));
+
+            var versionInfo = fixture.Create<VersionInfo>();
+            versionInfo.Version = new Version(1, 0).ToString();
+            versionInfo.Timestamp = DateTime.UtcNow.ToString(CultureInfo.InvariantCulture);
+
+            var packageInfo = fixture.Create<PackageInfo>();
+            packageInfo.Versions = new[] { versionInfo };
+
+            return packageInfo;
+        }
+
+        private JsonSerializerOptions GetTestSerializerOptions()
+        {
+            var options = new JsonSerializerOptions(JsonDefaults.Options)
+            {
+                WriteIndented = true
+            };
+
+            for (var i = 0; i < options.Converters.Count; i++)
+            {
+                // Remove the Guid converter for parity with plugin manager.
+                if (options.Converters[i] is JsonGuidConverter converter)
+                {
+                    options.Converters.Remove(converter);
+                }
+            }
+
+            return options;
+        }
+
+        private (string TempPath, string PluginPath) GetTestPaths(string pluginFolderName)
+        {
+            var tempPath = Path.Combine(_testPathRoot, "plugin-manager" + Path.GetRandomFileName());
+            var pluginPath = Path.Combine(tempPath, pluginFolderName);
+
+            return (tempPath, pluginPath);
         }
     }
 }
diff --git a/tests/Jellyfin.Server.Implementations.Tests/Test Data/Updates/manifest-stable.json b/tests/Jellyfin.Server.Implementations.Tests/Test Data/Updates/manifest-stable.json
index fa8fbd8d2c..57367ce88c 100644
--- a/tests/Jellyfin.Server.Implementations.Tests/Test Data/Updates/manifest-stable.json	
+++ b/tests/Jellyfin.Server.Implementations.Tests/Test Data/Updates/manifest-stable.json	
@@ -681,4 +681,4 @@
             }
         ]
     }
-]
\ No newline at end of file
+]