The story takes place immediately after the events of Ori and the Blind Forest and is narrated by the Spirit Tree. 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 it 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, but with the waters of Niwen unclean, Ori must set the wheels of The Wellspring back into motion to enter them. Kwolok also gives Ori a wisp, the Voice of the Forest, to guide them on their journey. Meanwhile, Naru and Gumo head off to Niwen via a raft to find Ori and Ku. Upon setting The Wellspring's wheels back into motion, clearing Niwen's water, Ori enters the Silent Woods and reunites with Ku, but the pair encounters Shriek, a deformed, vicious owl who was an orphan at birth and rejected by the rest of her kind, ruling over the Silent Woods and terrorizing Niwen. Shriek attacks Ori and puts Ku in a coma.
After Ori mourns Ku's state, Kwolok explains that the Voice of the Forest is not at full power and cannot bring Ku back in its current state. Due to the Spirit Willow's prior passing, the light that it carried was shattered into five wisps that scattered across Niwen, leaving the forest vulnerable to corruption and decay that killed the Willow's guardian spirits and Shriek's parents before her birth. Kwolok tasks Ori with seeking the other wisps of the Spirit Willow's light: the Memory, Eyes, Strength, and Heart of the Forest, and merge the four with the Voice to reform the tree's light. Kwolok leaves his marsh to help Ori with locating one of the other wisps, but his body is forcibly taken over by the Stink Spirit, a creature born out of the forest's decay whose body jamming the wheels of The Wellspring had been the cause of its non-functionality. Ori breaks the creature's control over Kwolok, allowing for him to kill it, but their fight leaves him mortally wounded. Before dying, Kwolok pleads to Ori to restore and protect Niwen in his place.
Ori eventually finds all five wisps and merges them together to reform Seir, the Golden Light. Ori and Seir head to the Spirit Willow and Seir revives it. However, the tree tells Ori its time has passed and can no longer carry Seir, asking Ori to merge with the light to restore Niwen, though Ori would have to leave its previous life behind. With that, the Spirit Willow dies for good, and Seir is returned to Ori, but before Ori has a chance to merge with it, Shriek appears and snatches it. Ori defeats Shriek, who returns to the Silent Woods to die under the wings of her parents' petrified corpses.
Ori finally merges with Seir, healing Niwen and reviving Ku with her damaged wing restored in the process, which Naru and Gumo arrive in time to witness. Ku, Naru, and Gumo find where Ori and Seir merged, and discover a Spirit Tree beginning to grow there. They help the tree flourish and continue their life as a family together, as it is revealed that it was the new Spirit Tree that was narrating the story and was Ori all along, retelling the events leading up to when it merged with Seir. Eventually, the tree completely grows and life begins anew as a new spirit guardian falls from it.
