Some years after Lord British has returned to power, the Avatar is captured and tied on a sacrificial altar, about to be sacrificed by red demon-like creatures, the gargoyles. Three of the Avatar’s companions, Shamino, Dupre and Iolo, suddenly appear, save the Avatar and collect the sacred text the gargoyle priest was holding.
The Avatar’s party flees through a moongate to Castle Britannia, and three of the gargoyles follow. The game begins with the player fighting the gargoyles in Lord British’s throne room. After the battle, the Avatar learns that the shrines of Virtue were captured by the gargoyles and he embarks on a quest to rescue Britannia from the invaders.
This game ended the use of multiple scales; in earlier games a town, castle, or dungeon would be represented as a single symbol on the world map, which then expanded into a full sub-map when entering the structure. In Ultima VI, the whole game uses a single scale, with towns and other places seamlessly integrated into the main map; dungeons are now also viewed from the same perspective as the rest of the game, rather than the first-person perspective used by Ultima I-V.
The game kept the basic tile system and screen layout of the three preceding parts, but altered the look into a much more colourful and detailed oblique view, to take full advantage of the newly released VGA graphics cards for PCs. Non-player characters had their portraits shown when talked to, something that would not have been feasible on the classic 8-bit Apple II.