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Humans live in the world of Assiah, demons in Gehenna. The two dimensions are not meant to interfere with each other, but demons still possess creatures in Assiah in spite of this. The humans who can fight these demons are known as exorcists. Rin Okumura is a boy who bears the curse of being Satan's illegitimate son. His foster father sacrificed himself to save him from demons. To avenge his foster father's death as well as to prove himself, Rin decides to follow the path of an exorcist and defeat his own father, Satan. To hone his raw skills, Rin enters True Cross Academy to train with other exorcist candidates.
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.
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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.
Rin and his classmates succeed at the task gave to them by their teachers, but the camp is attacked by Amaimon, who holds Shiemi hostage to force Rin to fight. Having no option but to go full force against Amaimon, Rin is forced to reveal his secret by exposing his true form in front of his friends. With the other Exwires fleeing astonished after learning the truth about him, Rin easily overpowers Amaimon, but loses control of his flames and goes on a rampage. The Demon-Slaying Blade is cracked in the process.
Shiemi manages to calm down Rin, who is captured by Arthur Auguste Angel, the current paladin, and taken to the True Cross Order Headquarters in the Vatican along Shura and Mephisto Pheles. Meanwhile, Rin's classmates become astonished when Yukio reveals to them that he and his brother are sons of Satan, but offer their help regardless, and they set for Kyoto looking for the descendant of the swordsmith who forged the Demon-Slaying Blade to have it fixed. Before the Order's upper echelons, Mephisto states that his reason for keeping Rin alive is to have him confront Satan, and just when he is trying to convince them to agree to his plan, an enraged Amaimon breaks in, eager to confront Rin once more.
Easily breaking through all defenses, Amaimon reaches the room where Rin is being held and Mephisto convinces the Grigori to agree with his plan. Using the reforged Demon-Slaying Blade brought by his classmates, Rin defeats Amaimon and the Grigori decides that he has six months to pass the Exorcist authorization exam, thus he begins a special training to learn to control his flames. Despite they helped Rin by having his sword fixed, some of his classmates still has some mixed feelings about him after learning of his connection with Satan, the most awkward of them being Konekomaru, who is approached by a dark presence attracted by his fear.
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The Exwires learn that Kamiki's birthday is coming and they decide to make a surprise party to her. Despite all their efforts to make the party a secret, Kamiki ends up figuring the truth and claims that it should also be dedicated to those whose birthday already passed too. In the end, the party becomes a celebration to everyone's friendship.
Rin and Yukio find that their friends from the monastery where they were raised where attacked by a masked individual who covered their entire bodies with an seemingly indestructible spider web. While pursuing the culprit, whose objective is to attack anyone related to the son of Satan to make him suffer, Yukio stumbles into Neuhaus who flees without further explanation. Despite having his sword sealed by the web, Rin insists to go after the masked one but is held back by Yukio and Shura, until he gets word that his Suguro, Renzo and Konekomaru are being attacked too and rushes to help them. By managing to control his flames properly, Rin defeats the attacker, who flees thanks to Neuhaus who reveals her to be his wife, and safely releases his friends.
Shiemi in the Exorcist Shop finds a woman lying unconscious in their garden. Meanwhile, Yukio meets an old man on a train, who claims to be his grandfather, and reveals the truth about their Mother who was burnt alive by the Vatican proclaiming her to be a witch. He takes Yukio to a secret anti-demon Dragoon Laboratory and suggests Yukio to join him now that Shiro is dead and Mephisto has been arrested. Prof. Neuhaus is being interrogated in the Academy's Great Cell by Shura where he tells everyone(including Rin) that his wife,(Masked Man) Michelle, is nothing but a corpse with a certain demon in her body, intending to kill Satan but she was not resurrected from death by him. Rin finds out the woman in the garden to be Neuhaus' wife but Shiemi stops him from killing her. Paladin Angel appears in the garden to kill the demon but confronts Rin. Later, Michelle dies protecting Rin from the Order.
Ernst takes over as the True Cross' newest leader and appoints Yukio as the new Paladin. Armed with special weapons that drain the blood of the demons killed with them, the exorcists take part in a widespread crusade to erase all demons from Assiah. Rin and his friends start questioning why the order decided to take such extreme measures, but Yukio is determined to accomplish his task as Ernst claims that it is all part of their plan to destroy Gehenna, and with the Demon world vanquished, both he and his brother would become completely human again. However, Ernst's real objective is revealed when he uses Rin as a human sacrifice to bring Satan to the Human World, using Yukio's body as a vessel.
Ernst's plan to destroy Gehenna backfires when Satan reveals to Yukio the truth behind his and his brother's origin before taking posession of his body.
Rin and his companions manage to flee from Satan who starts destroying the True Cross Academy with his flames. Knowing that Satan still stands beside the Gate because Rin has the power to destroy it, Shura comes up with a plan to distract him to give Rin an opening to do it, while the other students help evacuate the school. Their plan fails when Shiemi intervenes trying to dissuade Yukio with no success, but Rin manages to have his brother regain conscience and expel Satan from his body. However, the gate keeps getting stronger and it will not be long for Gehenna and Assiah to merge into one single realm.
Rin, Yukio, Shura and Arthur join forces to bring down the Gehenna Gate with no success. Meanwhile, demons keep coming through it and giving a hard time to the other Exorcists until the Esquires come with a plan to open a gate to Vatican, where is already daytime, and reflect the sunlight there to the Academy where is nightime to weaken the monsters protecting the Gehenna Gate. Rin and Yukio manage to seize these opportunity and when both unlock their demonic powers together, they fly through the gate and destroy it. One month later, things return to normal at the Academy and the Okumura twins return to the cave where they were given birth and pay a visit to their mother's grave. After visiting their mother's grave, they meet an "evil spirit" in a highway. Rin appears from a highway cave with Kuro. The evil spirit then attacks Rin and Yukio. Rin destroys the evil spirit's first body and then the spirit takes control over a truck. Yukio shoots at the truck, Rin tell hims that there is somebody in the truck. Yukio says its just a dead corpse, but Rin believes the driver is still alive and that it's an Exorcist's job to protect people and defend against demons. He tells Yukio and Shura to find its weak point and charges after the monster.
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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.
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