When the village of Vellie is attacked by a band of pirates, he sets out on a journey with Geddy to save the village, and the rest of the world as they know it. Geddy is a human who serves as the Vellie Guard. He spirals quickly into a small bout of depression, but is helped out of it by his self-proclaimed friend Geddy. As such, Otus is not seen as a suitable successor to the owl name. Otus is looked down upon by the other members of Vellie, because he is accident-prone. He is given an owl cloak by Asio, which gives him the ability to fly. The game begins with a scene including Otus's mentor Asio, who is training him to be an owl.

The main character is called Otus, who is mute. The areas surrounding Vellie and Advent contain old relics and temples in them from the time the ancient owls were larger in number and ruled the land. The owls do not naturally have the ability to fly like their wild counterparts, but with the help of an owl cloak, they are given the ability to fly. Vellie is located near the floating city of Advent which is their capital. The village is made up of many different islands, and is populated with humans and owl-humanoid creatures alike. Owlboy takes place in the floating settlement of Vellie. When Otus' village is attacked by a band of pirates, he sets out on a journey to save it from them, and uncovers the lost truth of the Owls. The player controls a boy named Otus, who is a member of an owllike humanoid race called the Owls.

Owlboy is set in the land of the sky the islands of the world below have been separated by a catastrophic event. As the game progresses, Otus gains allies that accompany him during his journey, each having their own weapon with exclusive properties. These objects vary in use, but are mainly used as ranged weapons, thrown weapons, and puzzle-solving tools. The player controls Otus, who is capable of flying and carrying objects during flight.

Owlboy plot