Naija lives in a city on a rock floating high in the sky. She dreams of the ocean, painting pictures of the distant fascination she can never reach. One day the city is hit by meteors and she tumbles down into the endless depths of the object of her fantasy: the ocean. Instead of drowning she wakes up, transformed to fit her new environment: a cave that serves as her sanctuary for a long time. There she learns of the verse, a harmony that flows through the underwater world of Aquaria. But eventually she leaves the cave, driven out by loneliness (inspired by Metroid) and restlessness, wondering if she is the only one of her kind.
Aquaria is a 2D side-scrolling shooter with a focus on exploration. Naija can freely roam her underwater world with fluent movement, reminiscent of Ecco the Dolphin. She soon meets a dark creature that shows the hidden dangers Naija will have to face if she continues her quest. Naija is moved around large maps at a constant speed. Clicking away gives her a speed boost and she can also cling to walls to launch herself with a sudden burst, or break through the ocean surface.
To face dangers, Naija has to use the power of the verse. By right-clicking on her, eight notes of different colours are shown, and clicking them triggers a chant. By chanting the right tone at certain plants, Naija can collect items, and learn spells and recipes. In the style of Loom or The Legend of Zelda: Ocarina of Time, the notes can be combined into songs to cast spells. These form shields, can be used to lift objects or change Naija to different forms with new abilities giving access to new locations. Right-clicking interacts with the environment and is used for attacking. In an items menu food and other objects can be used or cooked in combination to form new ones. During the game Naija also meets four pets that assist her and there are ancient turtles she can use to travel over large distances.
The different environments are linked from Naija's home, a central hub. Hidden treasures found while exploring are used to decorated the cave or can be used as a costume. During gameplay, a mini-map is shown in the bottom right corner and it can be enlarged to a full map. The game can be saved using red crystals scattered around the areas and it includes a level editor to create new environments and modifications.