Mona De Lafitte, the game's protagonist, is a young and talented Parisian opera student who becomes the object of obsession for a rather pathetic vampire. As a result, Mona is swiftly kidnapped and taken to his castle in Draxsylvania, where she is turned into an undead vampire. Mona must find a way to return home and fulfill her dream of becoming a famous opera singer, while also dealing with the unfamiliar problems inherent in her new condition.[1] Mona is not alone throughout the adventure however, but is followed by her newly acquired and sarcastic sidekick, Froderick the bat.

The game will be divided into three chapters, the first of which will take place in Castle Warg — the home of her kidnapper Shrowdy von Kieffer and his mother the Baroness Vasilia von Kieffer. The second chapter will largely take place in the town of Vlad's Landing, while the third will center about the castle of Dr. Riga Mortis. Little else is currently known about these latter two chapters of the game, other than that the player will be allowed to control Mona's companion Froderick during the final chapter, as at certain other points in the game

A Vampyre Story was created by a number of former LucasArts adventure game developers, and so is understandably similar to some of their previous classics (such as The Curse of Monkey Island (CMI) or The Dig) in presentation and style.[3][4] As such, the game will utilise a point-and-click interface with a context-sensitive radial cursor, much the same as CMI:[5] upon clicking an interactive item, a graphic menu will appear around the object, displaying the available actions and abilities. As the game progresses, Mona will gradually learn how to use her new supernatural abilities. Consequently, her newfound powers (and weaknesses) will play a large role in the game's puzzles, requiring Mona to use her abilities to overcome certain challenges and progress through the game.