Suguro's joint strategy pays off, and the Exwires have success in their sights! But then a gigantic moth demon (cuchi) appears, and attacks Rin the moment he lets his guard down!

Ernst is scheming to open the Gehenna Gate by using the blood of Rin, son of Satan. In order to protect his wounded older brother, Yukio offers to take his place.

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.

Satan has transformed himself into a gigantic Gehenna Gate, and is attempting to absorb all of Assiah. Rin and Yukio, joined by Shura and Angel, attack the gate. Meanwhile, at the school, the exorcists defend against a myriad of demons.

Hordes of demons are spilling out of Gehenna Gate, and are now indiscriminately attacking the people of True Cross Academy Town! Meanwhile, Rin has been rescued by Suguro and Shiemi and is starting to come to. What Rin sees when he awakens is...

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!

In light of the recent incidents, Mephisto is dismissed from his post as director. The Order’s Supreme Advisors are ousted as well, paving the way for Ernst to become Pope. And the newly appointed Preceptor of the Japan Branch is revealed to be...

Blacky went beserk when she heard the Father Shiro died and kept telling the exorcists that they were all lying about his death though only Rin could understand her (He said it may because they are both demons). When Yukio was about to use the item that Father Shiro gave him before if ever this scenario happens, Rin told him to let him calm Blacky down. In the end, Blacky accepted the fact that Father Shiro died and Rin and Yukio found out that the item that Father Shiro gave Yukio was actually his catnip wine.

The assailant has escaped, but things are just getting back to normal after the monastery attack. Just then, someone appears before Yukio!

Overwhelmed by his conflicting emotions, Yukio takes drastic measures, but Satan blocks him. After hearing from Shiemi about Yukio, Rin rushes out of the dorm to search for him. Assiah, the material world, is thrown into chaos as demons become more active. Mephisto is summoned to the prime minister's office and attends a press conference with the prime minister and all relevant parties to announce the existence of demons, which has never been publicly acknowledged until now. But who appears there is...

Fujimoto and his companions try their best to protect Rin from the demons who are after him, but he ends up posessed by Satan, the most powerful of the demons and Rin's father. Seeing his guardian taking his own life to protect him fron Satan, Rin decides to fight back by unlocking his demonic powers, even knowing that by doing it he would not be a human anymore.

Consumed by the power of the flames during his battle with Amaimon, Rin goes berserk! He regains control of himself once his power is exhausted...only to be captured then and there by the current Paladin, Angel!

The Exwires are tasked to look for the ghost of a child that is haunting Mephisto Pheles' amusement park. Rin and Shiemi manage to find the ghost first, but Shiemi ends up chasing it by herself while Amaimon, a higher demon and another son of Satan, steals Rin's sword and forces Rin to fight with him. Mean while another exorcist comes to defend him, and it is reveal to be an old friend of Rin's brother.

Using the Koma Sword, Shiro successfully seals Rin's demon heart. This separates Rin from his demonic nature and returns him to Yuri's arms. However, the respite is short-lived as Satan forcibly possesses the body of the Paladin Abel. Satan's love for Yuri has turned into obsession, but Yuri's words can no longer reach him. Satan explodes with emotions and attempts to take possession of Shiro's body. Shiro makes a bold move to prevent himself from being possessed, but...

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.

The first semester has ended, signaling the start of summer vacation for True Cross Academy students. But there’s no rest in sight for Rin and the other ExWires: first they must take part in a 3-day drill to prepare them for actual combat, under the guise of a camping trip out in the forest.

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...

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…!

Still troubled after her friend Paku decides to leave the Exorcist lessons, Kamiki gets involved in a fight with Bon and the entire class end up punished by Yukio. Just after Yukio leaves for a mission, the students are attacked by another ghoul and while trying to help the others, Rin learns that the monster was sent by one of his teachers who wanted to confirm that he is the son of Satan.

Yukio is arrested on suspicion of shooting Mephisto. After learning about Yukio's eye, Rin decides to escape from The Order with his brother. With the help of the Exwires and Amaimon, he heads off to rescue Yukio. Severely injured by the gunshot, Mephisto decides to abandon the barrier he placed on the artificial Gehenna Gate in order to maintain his possessed body. As a result, the gate opens completely, and a horde of demons emerge. The atmosphere of Gehenna thoroughly envelops Assiah...

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.

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

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.

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.

Lightning and Suguro bear witness to Section 13 as it appeared right after the Blue Night, and Mephisto reveals the truth about the research that was being conducted there. Meanwhile, Shiemi suddenly expressed her intention to decline to take the Exorcist Certification Exam and to leave the school.

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.

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.

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.

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...

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.

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.

Despite the success in taking control of the Far East Laboratory, the Illuminati remain a major threat. The Knights of the True Cross repeatedly hold discussions among the higher ranks to create countermeasures. Meanwhile, Rin and the other students are informed that the Exorcism Certification Exams will now be held sooner than planned. After the events in Shimane, Suguro struggles with the fact that he's lost sight of the reason for becoming an exorcist. However, Arch Knight Lightning is appointed as a new instructor at the Exorcist Cram School...

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.

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.

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

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...

The artificial Gehenna Gate has completely opened, throwing the material world of Assiah into utter chaos as many humans have now begun to see demons. Amid everything, Yukio leaves the Knights of the True Cross and heads for the Illuminati. Rin decides that he must learn the secret of their birth. He embarks on a journey 40 years into the past with Mephisto's guidance. Rin witnesses the fated meeting between two individuals – an orphan who lives in an abandoned factory named Yuri, and a test subject from Section 13 named Shiro.

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.

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...

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.

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…

Yukio wants to know the secret of their birth while Rin believes there is no need to know. As their ideas clash, Rin and the others head to Kyoto to attend the wedding of Juzo Shima and Mamushi Hojo.