Despite the success in taking control of the Far East Laboratory, the Illuminati remain a major threat. The Knights of the True Cross repeatedly hold discussions among the higher ranks to create countermeasures. Meanwhile, Rin and the other students are informed that the Exorcism Certification Exams will now be held sooner than planned. After the events in Shimane, Suguro struggles with the fact that he's lost sight of the reason for becoming an exorcist. However, Arch Knight Lightning is appointed as a new instructor at the Exorcist Cram School...

Ever since the strange phenomena occurred with his eye, Yukio decides to investigate the nature of the power that has manifested. He puts his own life on the line as he becomes devoted to the dangerous training…

Shura suddenly goes missing. However, based on her last traces, Mephisto deduces the high possibility that Shura has returned to her hometown in Aomori Prefecture. As such, he orders Rin and Yukio to go there and search for her. After investigating, the twins arrive at Lake Towada in Aomori. Shura was facing off against Hachirotaro Okami, a powerful Hydra who claimed the large territory centered at the lake and the surrounding areas. Hachiro and his snake companions urge Shura to fulfill her promise to him.

With the incident in Aomori concluded, things begin to calm down at the Knights of the True Cross Japan Branch. Lightning begins his investigation of the Illuminati with Suguro. Lightning suspects that there was something within the Japan Branch that was connected to the Illuminati and the "Blue Night." Meanwhile, after receiving Rin's confession, Shiemi worries that she doesn't understand the difference between "romantic love" and "friendship love." Unable to bear any further witness to this, Izumo makes a suggestion.

As Lightning continues to investigate the Blue Night, he notices the names of three people. After the Blue Night, three men left the Knights of the True Cross Japan Branch and became priests living at the Southern Cross Monastery, the place where the Okumura Brothers grew up. Lightning and Suguro visit the Monastery to get a firsthand account of what happened back then. Lightning, willing to take strong measures against those who remain silent, closes in on the mystery of the Blue Night...

The exorcists are busy dealing with the high-ranking demons that begin appearing in urban areas. Shura heads the forefront in Ikebukuro. The number of people who are able to see demons increases as a result of gaining a Temptaint, and the world falls into chaos. At the same time, Yukio threatens Suguro with his gun and tries to get him to learn about the details of Lightning's investigation. Yukio refuses to heed Shima's warnings and grows increasingly isolated. He returns to Tokyo for a mission and encounters Lightning

Yukio is arrested on suspicion of shooting Mephisto. After learning about Yukio's eye, Rin decides to escape from The Order with his brother. With the help of the Exwires and Amaimon, he heads off to rescue Yukio. Severely injured by the gunshot, Mephisto decides to abandon the barrier he placed on the artificial Gehenna Gate in order to maintain his possessed body. As a result, the gate opens completely, and a horde of demons emerge. The atmosphere of Gehenna thoroughly envelops Assiah...

According to the contract made between Hachiro and Shura's ancestor, Tatsuko Kirigakure, each generation of descendants is destined to die at the age of 30 in exchange for gaining power. Shura informs Rin and Yukio about her fate. She states that she has no regrets, but Rin is not convinced and suggests they defeat Hachiro. However, Hachiro then abducts Shura. Rin and Yukio make their way to Hachiro to save her, but they arrive to find Shura being controlled by Hachiro's hypnotic powers.

Overwhelmed by his conflicting emotions, Yukio takes drastic measures, but Satan blocks him. After hearing from Shiemi about Yukio, Rin rushes out of the dorm to search for him. Assiah, the material world, is thrown into chaos as demons become more active. Mephisto is summoned to the prime minister's office and attends a press conference with the prime minister and all relevant parties to announce the existence of demons, which has never been publicly acknowledged until now. But who appears there is...

With Yukio's clever wit, Rin and his friends are able to deceive Hachiro and successfully get him to break his contract with Shura. However, Hachiro loses all control in a rage, capturing Shura once more and heading toward the frozen lake. When the immortal Hachiro expresses his wish to die, Shura tells him they will sleep together forever at the bottom of the lake and embraces him. But as they sink into the lake, memories of the days she once spent with Shiro flash through Shura's mind.

Yukio wants to know the secret of their birth while Rin believes there is no need to know. As their ideas clash, Rin and the others head to Kyoto to attend the wedding of Juzo Shima and Mamushi Hojo.

Lightning and Suguro bear witness to Section 13 as it appeared right after the Blue Night, and Mephisto reveals the truth about the research that was being conducted there. Meanwhile, Shiemi suddenly expressed her intention to decline to take the Exorcist Certification Exam and to leave the school.

The artificial Gehenna Gate has completely opened, throwing the material world of Assiah into utter chaos as many humans have now begun to see demons. Amid everything, Yukio leaves the Knights of the True Cross and heads for the Illuminati. Rin decides that he must learn the secret of their birth. He embarks on a journey 40 years into the past with Mephisto's guidance. Rin witnesses the fated meeting between two individuals – an orphan who lives in an abandoned factory named Yuri, and a test subject from Section 13 named Shiro.

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!

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.

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.

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.

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.

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...

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 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.

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.

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.

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.