After his secret is exposed, Rin takes part in a special mission along Shura and Yukio to retrieve the "Left Eye of the Impure King", a demon relic that was stolen from the True Cross Academy's vault. In the occasion, they fail to retrieve it, but discover that the culprit is Saburota Todo, one of the exorcists in charge of the vault that was corrupted upon being possessed by a demon. After hearing that there was an attempt to steal the Left Eye's sister relic, the "Right Eye of the Impure King" in Kyoto, the Order sends a team there to investigate, including Shura, Yukio and the Exwires, who are in conflict after learning the truth about Rin.

The Exwires arrive at Kyoto, and Ryuji, Konekomaru and Renzo take the opportunity to reunite with their families, while Rin and the others tend to the Exorcists of the Myoda Sect, who got wounded guarding the Right Eye of the Impure King. In the occasion, Rin meets Ryuji's father, and learns that Ryuji is resentful of him, as despite being the leader of the Myoda Sect, he is not respected by the others, as he relegated his duties since the Sect, which was weakened after losing several of its members on the Blue Night, joined the True Cross Order. Meanwhile, Todo, with the Left Eye of the Impure King replacing his own, contacts his mole inside the Sect, planning another attempt to steal the Right Eye.

The Myoda Sect has an emergency meeting to discuss the failed attempt to steal the Right Eye of the Impure King and discover who among them is the traitor collaborating with Todo. In the occasion, suspicions were raised towards two of the sect's exorcists, Renzo's older brother Juzo and Mamushi as they were present at the scene and were Todo's students in the past, but the head priest, who did not attend the meeting, was counted as a suspect as well, much to Ryuji's anger. Meanwhile, Rin continues with his training to control his flames while trying to reconcile with his friends, who fear how the Myoda will respond once they learn that he is the son of Satan.

Who is betraying the Myoda sect? Without high priest Tatsuma in attendance, the general meeting falls into chaos and ends without a conclusion. As Suguro resolves to find and question his father, he witnesses someone sneaking into the Kyoto field office…

Although the traitor was revealed, the Right Eye of the Impure King has been stolen. While confronting Ryuji, Rin loses control of his blue flames in front of the gathered exorcists. In all of the commotion, Tatsuma slips Shura a letter addressed to Rin.

Shiro Fujimoto, Rin and Yukio’s adopted father, encountered Tatsuma Suguro while trying to take the demonic sword, Kurikara. Tatsuma’s letter reveals the circumstances of how the sword, which is the Myoda Sect’s main object of worship, came to Rin.

The Impure King has been revived! In his letter, Tatsuma asks Rin to use the Koma sword to fight, but will that even be possible? And to make matters worse, Mephisto suddenly appears with the news that Rin has been sentenced to death!

Miasma spreads through the streets as the exorcists begin to counter the Impure King’s growth. Rin leaves with the other students to find Tatsuma. Yukio is on the front lines, unaware his brother has left his cell, when he notices something strange…

“You despise your brother, don’t you?” Yukio is shaken as Todo tells him to admit his true feelings. Yukio reflects on the thoughts he’s had since an early age. Meanwhile, Suguro has inherited the Gouha-en, and with it, he and Rin head to the sporangium.

The sporangium has finally burst, revealing the Impure King. Assaulted by the miasma, Suguro barely maintains the barrier. And every passing moment brings him closer to his limit. Rin questions why he can’t draw his sword, even when backed into a corner.

Rin finally manages to draw the demon sword. Shura tells him to, “Win a place for yourself in this world!” However, there doesn’t seem to be a way to stop the Impure King’s overwhelming growth. And if Suguro’s strength fails, the barrier will collapse!

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 Okumura, a boy aiming to become an exorcist yet born the illegitimate son of the demon god Satan, advises his classmate Sei Godaiin, who begins to see demons. Despite Rin asking Ryuji Suguro and the other Exwires attending the Exorcism Cram School for a way to make demons invisible, he is unable to find a solution. Meanwhile, Rin is invited to dinner by Mephisto Pheles, the Preceptor of the Japan Branch of the Knights of the True Cross and director of the True Cross Academy. However...

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.

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.