Rin and his classmates Izumo and Shima are sent for their first mission as Exwires to a coast town aflicted by the presence of a Kraken. Izumo stumbles upon a boy whose father set to face the Kraken six months before and is still missing. The boy plans to enact his revenge against the creature as he believes it killed his father, but he and the Exwires find out what really happened when they encounter it, much to their surprise.

The Exorcism Cram School students are having a ball with Shima's birthday-based fortune-telling. When they discover that Izumo's birthday is coming up, they hit upon the idea of throwing her a surprise party!

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.

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.

Behind the façade of the Inari Tourism and Urbanization Project, the Illuminati gradually undermined the area. After learning about Izumo's past from Mike, Rin and the others head to Peace Town Inari, which they believe holds the entrance to the Illuminati's underground laboratory. Meanwhile, at the laboratory, Izumo is taken to a room where Michael Gedoin is waiting to undergo a complete medical examination. Izumo screams to create an uproar, giving her a chance to try and escape by summoning Uke and Mike. She runs away to get out of the underground laboratory – only for Renzo Shima to stand in her way.

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.

Having lost her family in a fire and with nowhere left to go, Yuri meets Shiro, who is on the run from Section 13. Shiro is brought back by the exorcists pursuing him, and he makes a request of Mephisto. Meanwhile, Yuri is taken to the Asylum, a school for exorcists-in-training, due to her ability to see demons. As he watches the two grow up, Rin witnesses the true nature of the Asylum and Section 13.

Shiro believes that an exorcist's duty is to destroy demons, while Yuri believes that an exorcist's duty is to help people, and advocates for building friendly relationships with demons. Shiro, irritated by Yuri's attitude, harshly confronts her. Time passes, and the two pass their Exorcist Certification Exams. Shiro finally achieves his dream of leaving the Asylum and begins living alone and indulging in his freedom. Yuri watches on in concern, but another mission puts the two at odds once more...

After his incarnation, Rinka absorbed knowledge, recognizing himself as the Demon God Satan.

A newborn Rin, covered in blue flames, attacked the surrounding exorcists one after another. Rin, shaken by the sight and on the verge of being overtaken by his demonic self, is sent to a certain place in the present by Mephisto. Meanwhile, Yukio, who has left the Knights of the True Cross, and Shima arrive at the Illuminati's aerial fortress, the Dominus Liminis. Accompanied by the executive in charge, Homare Todo, Yukio meets Lucifer. Simultaneously, someone from the Grigori Sedes comes to visit Shiemi.

Shiemi cheers up after Rin suddenly appears before her. After hearing Shiemi's voice, Rin regains consciousness and heads back to the past to see the events all the way through. In the past, Satan's possessed body progressively deteriorates, beginning to break down and go out of control. The Blue Night begins at last. As powerful clergy around the world are engulfed in blue flames one after another, the Myodha Sect in Kyoto, the Three Sages in the Vatican, Shiro and the Knights in the Japan Branch struggle against the dire situation.

Shiro offers to leave the twins with Mephisto under the assumption that he has a plan to raise Satan’s children.

The sight of a blue flame burning in the night sky is reminiscent of “Blue Night,” but has brought about a completely different result. Now that the incidents relating to the Impure King have been concluded, those affected are moving on.

Rin undergoes training to master his demonic flames, when a giant bird-like demon swoops in on him! After driving it away, all of the Cram School members are sent to investigate how the demon infiltrated the academy...

Rin and Yukio find that the responsible for their meals at the dormitory was Ukoback, a cooking familiar appointed by Mephisto Pheles to aid them. They also learn how Ukoback can be troublesome when he gets angry.

Yukio sets out to the school's Exorcist-only shop to stock on some supplies along with Rin. There they find that the owner's daughter, Shiemi Moriyama, is being afflicted by a demon that dwells in her family's garden and, to save her life, they confront it by themselves.

Having Shiemi as a new classmate, Rin's total disregard for classes brings forth the anger of another classmate of his, Ryuji Suguro, aka "Bon". After learning of Bon's story, Rin finds that they have more in common than he would like to admit.

Mephisto Pheles reveals to the students that the ghoul attack was actually part of the Esquire exam and how they dealt with the threat will count as part of their evaluation. Yukio confronts Neuhaus about his reasons to force Rin to use his demonic powers during the exam and he claims that all he did was under Mephisto's orders. However, it does not take much for Yukio to realize Neuhaus' real intentions.

As the hearing drags on, the Order finds itself unable to decide on Rin's fate, as Mephisto has proclaimed him to be "a weapon for counterattacking Satan." Just then, something happens…!

Southern Cross Monastery, where Rin and Yukio grew up, has come under attack by a mysterious assailant! Leaving behind these cryptic words: "I will never forgive anyone related to Satan," the masked assailant escapes...