Due to a recent spree of attacks by an escaped criminal, Hime Yarizakura begins to investigate the occurrences with her assistant, Kyōsuke Kishi. She enlists the help of Akina Hiizumi, Ao Nanami, and Kotoha Isone, who are preparing to welcome a new yōkai resident, Rin Azuma, a Jiang Shi, into Sakurashin. That evening, Hime confronts the criminal, Kosuke Yoshimura, who is holding Rin hostage, and Kosuke disappears when Hime attacks him. The following day, Kosuke holds V Juri F, a nurse, hostage, and demands that Hime comes to him. Hime does so and with Ao's, Kotoha's, and Kyōsuke's aid, they defeat Kosuke. Rin appears and holds Akina at gunpoint, revealing that Kosuke promised her revenge on the humans that abused her. Akina uses tuning to expel the yōkai from Kosuke's body, and when he offers to bring Rin to his office, she declines, claiming that she hates all humans.
Hime meets with Yūhi Shinatsuhiko, a tochigami, to discuss Rin's status in the city, and they decide to have her attend school and work in the city. Hime assigns Akina to be Rin's caretaker, but she quickly leaves. When she encounters Hime, she asks why Akina is allowed in the city, and Hime claims that Akina's tuning ability is necessary for the city's peace; however, Rin considers tuning murder. Elsewhere, Enjin Hiizumi, a wolf yōkai, attacks one of the Seven Pillars, the spiritual sakura trees that protect the city. Throughout the city, yōkai begin to lose control of their powers, and Hime confronts Akina, who is upset about Rin's belief that tuning is murder. Near Akina's office, Rin begins to lose control of her powers, and Akina uses tuning to expel the yōkai that was possessing her. The following day, a grateful Rin arrives at Akina's office to sell food.
Hime trains in her dojo with Kyōsuke, and recalls when her grandmother, the previous mayor of the city, died and left the title of mayor to Hime. At Akina's office, Hime starts to raise a dog named Silver, and determined to raise it well, feeds it ramen. After hearing a citizen comment on Hime's focus on raising Silver over her mayoral duties, Akina relates this to Hime, who claims that she can do both without complications. That evening, Silver goes into Akina's office and bites him. Furious, Hime hits Silver and he walks away dejectedly despite Ao's pleas. Enjin encounters Silver after attacking one of the Seven Pillars, and implants a yōkai into him, forcing Hime to fight him. After the yōkai gains control over Silver's body, Akina is forced to use tuning, which releases both Silver's and the yōkai's souls.
Akina and Hime discuss Enjin's possession of Gin Nanami, Ao's brother, with Yūhi, who claims that Gin's soul is likely destroyed. Elsewhere, Enjin realizes that he cannot use his full power because Gin's soul is still present in his body. Ao and Tōka Kishi, Kyōsuke's sister, prepare food for Hime on her business trip. When Akina searches for headphones for Hime, he finds a monkey statue that he won in a yakisoba-eating contest with Gin and Hime. That evening, Enjin attacks the barrier created by the Seven Pillars and passes through it. His associate, Eiji Shinozuka, is confronted by Kotoha, Ao, and Yūhi, who realizes that Shinozuka is a hanyō like Kotoha. Akina confronts Enjin, but is unwilling to use tuning on him after Enjin reveals that Gin's soul is still present in his body. Akina is saved by Yae Shinatsuhiko, Yūhi's sister, and Enjin retreats.
Hime returns from her business trip, and begins to broadcast a song of her own making throughout the city. Meanwhile, Akina meets with the Senior Council, which tells him to disregard that Enjin is in Gin's body. Afterwards, Akina meets with Yae, and tells her to keep his encounter with Enjin a secret. Hime, Ao, Kotoha, Kyōsuke, and Tōka agree to supervise a daycare center, but are unable to control the children until Ao uses her telepathic abilities to play with the children. When Ao reads the mind of Junta, a reclusive child, she accidentally reveals a promise he made with his missing father, and Junta runs away. Distressed, Ao refuses to use her telepathic abilities. Akina and Hime manage to find the boy's father, and Ao apologizes to Junta. As Ao relaxes on one of the Seven Pillars, she sees Enjin hovering in the sky.
Enjin disappears and Ao relates the incident to Akina, who asks him to keep it a secret. Enjin begins to experience pain as Gin's body is resisting him, and he leaves Shinozuka to do what he pleases. Kotoha is planning a trip to Germany and a karaoke party with her friends, and Hime asks her to be her training partner. During the training, Hime pierces Kotoha's airplane ticket to Germany with her spear. Furious, Kotoha conjures a 88 mm gun. Kyōsuke blocks the shot, and Kotoha apologizes to Hime. That evening, Shinozuka kidnaps Kotoha's friends, and lures her to the river. Although Kotoha attempts to fight him, he dodges all of her attacks, and attempts to convince her to join him due to the abuse she received from humans in the past for being a hanyō. Hime arrives, reminding Kotoha that she is a human to the core, and Shinozuka retreats.
The townspeople of Sakurashin begin to prepare for the yearly festival honoring the Seven Pillars, and Akina and Hime, as the representatives of the Hiizumi and Yarizakura families respectively, are the key participants. In the ceremony, Hime carries the Dragon Spear into a shrine around one of the Seven Pillars and prays for the continued safety of the town. Following the ceremony, Akina and Hime join the party at Akina's office, where all the participants become inebriated on the alcoholic yōkai water. That morning, Enjin informs them that he has kidnapped Ao, and Akina, Hime, Kotoha, and Kyōsuke go to the shrine to meet him.
Enjin demands that Akina open the entrance to the shrine, and Hime attacks him. Kotoha and Ao begin to fight Shinozuka, who manages to dodge all of Kotoha's attacks. Using the telepathic abilities of Gin's body, Enjin realizes that Hime is unwilling to seriously fight him because he is inhabiting Gin's body and overpowers her. Realizing that Hime cannot defeat Enjin, Yae decides to join the fight, but Mariabelle, Yūhi's assistant, reveals that Yūhi has forbidden her from interfering. Enjin forces Akina to open the entrance to the shrine by holding Hime hostage, and Akina does so. Yae throws one of her swords into Enjin's back, but allows him to enter the shrine, where he starts to force the tree to bloom. To stop the process, Hime uses the Dragon Spear to remove part of the tree.
Hime meets with the Senior Council, and discovers that one of its members is severely injured, as all of the members of the Senior Council are linked to the Seven Pillars. Meanwhile, several yōkai begin to lose control of their powers. Tōka accidentally uses her oni powers to break a car, and is hospitalized. Kyōsuke confronts Akina, accusing him of lacking the resolve to remedy the situation by using tuning on Enjin. Ao attempts to visit Hime, but finds her furiously training. Enjin recalls the time a member of the Hiizumi clan used tuning on him after he claimed Sakurashin should be a city only for yōkai. Ao confronts Akina and tells Akina that he should use tuning on Enjin regardless of the danger to Gin's soul. The following day, Akina and Hime meet with the Senior Council members, who order them to cut down the Seven Pillars.
The Senior Council reveals that if the Seven Pillars are cut down, the city members will have to flee, but a portal that connects the human world to the yōkai world will not be created. When the townspeople question the decision, Hime is unable to calm them. On her regular rounds throughout the city, she learns that Akina has sent out recommendations to the townspeople to hide in safe locations, and she accuses him of lacking the resolve to defeat Enjin. A pair of giant yōkai attack, and Hime attempts to defeat one of them by herself, but is defeated. Akina, Kyōsuke, and Kotoha defeat both of them, and Hime is hospitalized. Meanwhile, the Seven Pillars start to grow, and Kyōsuke orders that the townspeople abandon the area. In the hospital, Hime tearfully confides to Akina that she is too weak to save the town by herself, and Ao tells her to allow her friends to help her.
Ao and Kotoha take a car and begin to search for the source of the yōkai energy that causes the Seven Pillars to grow, and Akina and Kyōsuke fight the yōkai appearing in the city. Hime attempts to leave the hospital to help, but Juri refuses to allow her to leave, citing her injuries. When she awakens later, Jinroku, an elderly citizen, gives her the head of the previous generation's Dragon Spear. As she leaves the hospital, she finds several townspeople who tell her that they want to fight the invading yōkai to save the town. Ao and Kotoha are nearly overwhelmed by the yōkai shadows appearing around them, but Yae saves them. Akina and Kyōsuke encounter Shinozuka and begin to fight him, and they are picked up by Ao and Kotoha, who reveal that the source of the yōkai energy is the tower in the center of the town. Kotoha conjures a railroad gun to attack the tower. Enjin goes to one of the Seven Pillars and forces it to bloom.
With the Dragon Spear, Hime begins to fight Enjin. When Akina arrives, however, he is still unwilling to use tuning on Enjin. Enjin travels to the meeting place of the Senior Council, and threatens to kill them. Yae arrives to fight him, but Yūhi tells her to allow Hime to fight him. Elsewhere, Kotoha fights Shinozuka, and after he overpowers her, Kyōsuke begins to fight him. After Kotoha distracts Shinozuka, Kyōsuke defeats him by trapping him behind a car. Hime continues to fight Enjin, who manages to cut her scarf using his scythe. In response, Hime uses the full power of the Dragon Spear to blow away all of the sakura petals on the Seven Pillars, and knocks Enjin into Akina, who uses tuning on him. Freed from Enjin, Gin thanks Akina and Hime before his spirit is sent back to the yōkai world. The following day, Akina repairs Hime's scarf and returns it to her.