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.

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.

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.