The film will be made up of two stories: "Ishi Okoshi" and "Ayashiki Raihousha." In "Ishi Okoshi," Natsume meets a small youkai called Mitsumi in a forest. Mitsumi is entrusted to wake up the divine youkai "Iwatetsu" from its deep slumber. Mitsumi weighs on Natsume's mind, so he sets out to help Mitsumi with his task.
In "Ayashiki Raihousha," a mysterious visitor appears in front of Tanuma. Nearly every day, the visitor visits Tanuma, talks to him a little, and then leaves. Natsume, who knows the visitor is a youkai, worries for Tanuma, but Tanuma enjoys these exchanges with the youkai. The youkai means no harm, but Tanuma's health slowly starts to deteriorate.

Natsume has been busy, navigating between humans and Yokai when he coincidentally reunites with an old classmate, Yuki. It brings back painful memories of a certain Yokai. Meanwhile, Natsume also became acquainted with Yorie Tsumura, a woman in the memories of a Yokai whose name he had returned. Yorie knew much about Reiko, but now lived a peaceful life with her only son, Mukuo. Being with this family was comforting for Natsume, but apparently a mysterious Yokai has been lurking in their town. On the way back from investigating, a “Yokai seed” that had latched itself to Nyanko Sensei drops into the Fujiwaras’ garden and grows overnight into a fruit tree. When Nyanko Sensei eats a fruit that is somehow shaped like himself, he suddenly splits into three!