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.

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.

Rin and Kamiki are attacked by an unknown enemy and Mephisto Pheles orders the Exwires to check the barriers protecting the school looking for any breach. The enemy is revealed to be a demon who took advantage of Konekomaru's fears to infiltrate the Academy. Meanwhile, Shura locates a hidden door leading to a suspicious abandoned lab. When Konekomaru's heart succumbs to the demon, his friends rush to help him, and Rin manages to slay the monster and save his life. Ashamed of causing so much trouble, Konekomaru decides to leave the Academy and return home, but Rin and the rest of his friends reach him before he departs and convince him to stay.

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.

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.