Rin Okumura is a teenager with a natural gift to get himself in trouble. Despite that he tries his best to meet the expectations of his twin brother Yukio and Priest Shiro Fujimoto, who acts as their guardian, until he finally learns about the dark secret behind his origin.

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.

As part of his training to become an Exorcist, Rin gets himself enrolled at the True Cross Academy. On his first day of classes, Rin becomes shocked to know that his twin brother Yukio is already an Exorcist and will be one of his teachers.

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.

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.

Eager to make new friendships, Shiemi asks her classmate Izumo Kamiki to be her friend and she pretends to agree, but Rin soon realizes Izumo is just taking advantage of Shiemi's kindness instead. Later, the students are reunited at the old dormitory to take part in the Exwire exam, where a demon attacks Izumo and her friend Paku by surprise and it's up to Rin and Shiemi to protect them.

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.

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.

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.

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 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.

Shura Kirigakure, a high level Exorcist and former apprentice of Father Shiro was acting as one of Rin's classmates tasked to investigate his connection with Satan. With orders to kill him if it were proven true, she is divided between fulfill her obligations and follow Shiro's request to look after Rin in his place if something would happen with him. Her doubts are cleared when she confronts Rin and finds that Shiro was actually raising him like a son instead of a weapon.

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.

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!

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!

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…!

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...

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!

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...

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

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...

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.

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...

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.

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.