Después del incidente de Kioto, la vida de Rin vuelve a la "normalidad". Aunque poco después recibe una carta de Mephisto que lo cambiará todo.

Yukio Okumura, Rin's younger twin brother and Intermediate Exorcist First Class, is summoned to a high-level inquiry meeting of the True Cross Order to be questioned about Saburota Todo, the mastermind behind the resurrection of the Impure King. Suspicious of the imposing atmosphere, Yukio recalls the words of his late adoptive father, Shiro Fujimoto. Meanwhile, the Exwires are tasked with exorcising "Mayuko of the Toilet." However, Izumo Kamiki holds a certain grudge against Shiemi Moriyama.

True Cross Academy is busy with preparations for the school festival. Renzo Shima and Rin try to find partners to attend the music festival and dance party with, but they are continually rejected. Unwilling to give up, Rin attempts to invite Izumo. But she flat out declines because the annual Exorcist Certification Exam is approaching. However, Shiemi, who has passed the school's transfer exam and has become their classmate, appears before a completely depressed Shima and Rin.

Arthur A. Angel and Lightning capture a spy hiding among the Knights of the True Cross and learn that the secret society, the Illuminati, is planning to abduct someone for a certain project. And now, the time for their plan is at hand. After hearing the news, Shura Kirigakure gathers the Exwires. Meanwhile, Izumo confronts Takara and angrily explodes when she sees a particular stuffed animal in his hands...

Every branch of the Knights of the True Cross is thrown into chaos as Lucifer, the King of Light, declares war. At the same time, Yukio, Rin, and the other Exwires leave for Izumo's hometown in Shimane Prefecture to bring Izumo and Shima back home. Izumo has been kidnapped and confined in the Far East Laboratory, controlled by the Illuminati. As Izumo awakens, she finds Shima wearing an Illuminati uniform. Then, she also meets someone with whom she shares a deep connection.

Takara summons Izumo's familiar, Fox God Mike, to talk about the past surrounding the Kamiki family and the Inari Taisha Shrine. Coming from a long line of shrine maidens, Tamamo, Izumo and Tsukumo's mother, serves as the head of the family who must bear the burden of controlling the fox demon, Nine Tails. Although Izumo possesses excellent divine power as a shrine maiden, she has no one she can rely on in her private life – she spends her days with her boisterous mother and younger sister. Those days fell into ruin when the Inari Light Foundation appeared and made its move.

Michael Gedoin, lost in his admiration and adoration for Lucifer, takes further action to ensure the success of his Elixir research. He devises a plan separating Rin and his team – leaving each member to fend for themselves. Although Rin faces off against a giant, grotesque Zombie in the underground laboratory's container, he hesitates to use his sword against it when he realizes the Zombie is a human corpse possessed by a demon. Yukio, Suguro, Shiemi and Konekomaru each must face off against their demons in the laboratory alone...

With the laboratory container now destroyed, Rin and the rest of the team were able to regroup, but Michael Gedoin sets a bloated Zombie to attack them. Gedoin talks about how the Far East Laboratory is the central hub for the Elixir of Immortality experiments – exposing the truth about Peace Town Inari and enraging everyone in the process. Then, Izumo appears – heading against her will to undergo the surgical transplant of Nine Tails. Rin breaks out his Koma Sword to save Izumo. Rin punches Shima, sending him flying, for trying to prevent Rin from helping her. Rin extends a helping hand to Izumo, but...

Forcibly possessed by Nine Tails, Izumo strains her energy to cry for help as the demon's power overwhelms her. Rin answers Izumo's cry for help, exorcises the bloated Zombie and finds himself standing in the way of Michael Gedoin. Gedoin, confused and impatient with the unexpected situation, unleashes more Zombies on Rin and the others to buy time. As Yukio and the rest of the group come rushing to fight back, Izumo begins to be swallowed up by Nine Tails' madness, which she cannot subdue and is losing control.

Izumo and the rest of the team succeed at thwarting the threat of the Illuminati, with the help of her mother, Tamamo. As the Knights of the True Cross gain control of Inari, the once-continuous turmoil and fighting finally calm down throughout the land. However, Renzo Shima leaves with the Illuminati as a member of their team. Suguro tries to explain that Renzo was a spy for the Illuminati to his elder brothers, Juzo and Kinzo, who've come to help from the Kyoto Branch – only to learn of an even more shocking truth from Juzo.

Shima returns home despite everyone thinking he had severed ties. Lightning questions his motives. Mephisto plans to face off against Lucifer. Amid these turns of events, Yukio hides that he met Lucifer in person in the Illuminati's underground facility, but Shima knows the truth. A sense of great unease grows stronger in Yukio's heart – Shima advises him to talk to somebody about it. In the meantime, Mephisto arranges for Rin and the rest of the crew to rest and relax at a spa resort in gratitude for their hard work.