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.

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 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.