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.