The story takes place immediately after the events of Ori and the Blind Forest and is narrated by the Spirit Willow in the forest of Niwen. Kuro's last egg hatches, giving birth to a baby owl whom Ori, Naru, and Gumo name Ku and raise as part of their family. Being born with a damaged wing, Ku cannot fly until Gumo affixes Kuro's feather to it. Ku and Ori go on a flight that ends up taking them out of Nibel and into Niwen, where a storm separates them. Ori's search for Ku eventually leads them to Kwolok, a toad looking over the Inkwater Marsh and some of the inhabitants of Niwen, the Moki. He tells Ori that Ku is in the Silent Woods, the Moki's former home now turned into a desolate graveyard of owls.
The player controls the titular Ori, a white guardian spirit. As Ori, players must jump, climb, glide, and swim between various platforms to solve intricate puzzles. Gameplay unfolds in the form of a Metroidvania, with new abilities and upgrades allowing players to unlock previously inaccessible areas of the map. Some of the foundational gameplay elements were inspired by the Rayman and Metroid franchises. Unlike its predecessor Blind Forest, Will of the Wisps relies on autosaving rather than manually placed "soul links". The sequential upgrade system of the first title has been abandoned for a system of "shards" , which can be purchased or found throughout the game to upgrade or modify Ori's stats and attacks. Ori's attacks can be managed via a convenient radial menu, and orbs to increase Ori's health and energy can be found throughout the map.