Exploring various dungeons is a major component of the game-play in Fairy's Rule. The player will have to navigate a small variety of dungeon environments in order to complete the game. All dungeons can be completed with the basic platforming mechanics, on top of any progress made in the course of getting to those levels, but spending resources on certain exploration skills (ie: swimming, climbing, flying, jumping) can allow the player to reach extra treasures, hidden exits, lore, or other bonuses.

In addition to the treasure that the fairies seek to reclaim, dungeons generally contain puzzles, traps, mycelial networks, and a variety of Non-Player Characters.

The dungeons in Fairy's Rule are procedurally generated each time the player enters. This is not because of the nature of the world, or a curse on the dungeons, but simply because fairies in this world are too absent-minded to remember the layouts.