diff --git a/Content.Server.Database/Configuration.cs b/Content.Server.Database/Configuration.cs
index 1541b42ed8..6db9a594d3 100644
--- a/Content.Server.Database/Configuration.cs
+++ b/Content.Server.Database/Configuration.cs
@@ -1,4 +1,5 @@
-using Microsoft.EntityFrameworkCore;
+using Microsoft.Data.Sqlite;
+using Microsoft.EntityFrameworkCore;
 using Npgsql;
 
 namespace Content.Server.Database
@@ -50,9 +51,10 @@ namespace Content.Server.Database
 
     public class SqliteConfiguration : IDatabaseConfiguration
     {
-        private readonly string _databaseFilePath;
+        private readonly string? _databaseFilePath;
 
-        public SqliteConfiguration(string databaseFilePath)
+        /// <param name="databaseFilePath">If null, an in-memory database is used.</param>
+        public SqliteConfiguration(string? databaseFilePath)
         {
             _databaseFilePath = databaseFilePath;
         }
@@ -62,7 +64,20 @@ namespace Content.Server.Database
             get
             {
                 var optionsBuilder = new DbContextOptionsBuilder<PreferencesDbContext>();
-                optionsBuilder.UseSqlite($"Data Source={_databaseFilePath}");
+                SqliteConnection connection;
+                if (_databaseFilePath != null)
+                {
+                    connection = new SqliteConnection($"Data Source={_databaseFilePath}");
+                }
+                else
+                {
+                    connection = new SqliteConnection("Data Source=:memory:");
+                    // When using an in-memory DB we have to open it manually
+                    // so EFCore doesn't open, close and wipe it.
+                    connection.Open();
+                }
+
+                optionsBuilder.UseSqlite(connection);
                 return optionsBuilder.Options;
             }
         }
diff --git a/Content.Server/Preferences/ServerPreferencesManager.cs b/Content.Server/Preferences/ServerPreferencesManager.cs
index 9b10a7e725..ac9e944f56 100644
--- a/Content.Server/Preferences/ServerPreferencesManager.cs
+++ b/Content.Server/Preferences/ServerPreferencesManager.cs
@@ -50,11 +50,11 @@ namespace Content.Server.Preferences
             {
                 case "sqlite":
                     var configPreferencesDbPath = _configuration.GetCVar<string>("database.prefs_sqlite_dbpath");
-                    var finalPreferencesDbPath =
+                    var inMemory = _resourceManager.UserData.RootDir == null;
+                    var finalPreferencesDbPath = inMemory ?
+                        null :
                         Path.Combine(_resourceManager.UserData.RootDir, configPreferencesDbPath);
-                    dbConfig = new SqliteConfiguration(
-                        finalPreferencesDbPath
-                    );
+                    dbConfig = new SqliteConfiguration(finalPreferencesDbPath);
                     break;
                 case "postgres":
                     dbConfig = new PostgresConfiguration(