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.