As Natsume's heart succumbs to the yokai from his past, he begins to recall distant childhood memories. Natsume is unsure where to call home, but while seeing the picture of his parents still brings pain, he reassures himself that he's no longer lonely.
Natsume decides to visit his old house one last time, and goes to get the key from a relative. Natsume used to live with the relative's family, and when he arrives, his memories come flooding back, along with a yokai he never thought he'd see again.
At a festival that takes place once every ten years, the gods Hozuki and Fuzuki compete for dominance. But this year, Hozuki is nowhere to be found. Natori is ordered to find him, while Natsume is enlisted to imitate the missing god.
Through a series of events, Natsume runs into Nanase of the Matoba clan. She's in search of a yokai she sealed away years before, and reflects on the days when she was still new to the act of exorcism.
The imprisoned Natsume is offered as a gift to a powerful yokai, Omibashira, but Tanuma and Natori come to his aid. As Omibashira begins devouring other yokai to gain strength, Natsume and the others attempt to flee.
Natsume finds himself trapped inside a glass bottle that was placed in his room by a yokai. Nyanko-sensei decides that only the owner of the bottle can open it. He decides to transform into Natsume and pretend to be him to avoid suspicion.
A former classmate of Natsume's, Yuriko, thinks back to when he first transferred to her middle school. Meanwhile, Natsume is reunited with a yokai he saved years ago, causing him to recall the same memories as Yuriko.
A yokai comes to Natsume seeking to use him as bait to lure out another powerful yokai. Before he'll help, Natsume demands to know what for, and the yokai recounts the story of when he met a human woman, long ago.
As Natsume treats an injured yokai, it accidentally poisons him. The yokai is part of a larger flock which is coming dangerously close to town. Natsume must also find the ring that a yokai has accused him of stealing, or suffer the consequences.
Hinoe and Misuzu head out in search of the monkey yokai leader to try and reclaim Natsume. Natsume has been imprisoned by Matoba, who wants him to join them. Natsume can't contain his anger, and makes a daring escape with Nyanko-sensei.
Natsume has a dangerous run-in with a group of yokai clad in monkey masks. They lure him into their forest lair, where the border between the human and yokai world is blurred. It's here that Natsume once again encounters the Matoba clan of exorcists.