Jiiiii～

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.

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.

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.

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...

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.

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.

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.

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...

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...

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.

Having lost her family in a fire and with nowhere left to go, Yuri meets Shiro, who is on the run from Section 13. Shiro is brought back by the exorcists pursuing him, and he makes a request of Mephisto. Meanwhile, Yuri is taken to the Asylum, a school for exorcists-in-training, due to her ability to see demons. As he watches the two grow up, Rin witnesses the true nature of the Asylum and Section 13.

Shiro believes that an exorcist's duty is to destroy demons, while Yuri believes that an exorcist's duty is to help people, and advocates for building friendly relationships with demons. Shiro, irritated by Yuri's attitude, harshly confronts her. Time passes, and the two pass their Exorcist Certification Exams. Shiro finally achieves his dream of leaving the Asylum and begins living alone and indulging in his freedom. Yuri watches on in concern, but another mission puts the two at odds once more...

Nine years have passed. During that time, Shiro, Yuri, Rick and the others gained experience and grew up. Meanwhile, in Section 13, Elixir experiments continued. Although Amaimon successfully possesses a new body, Lucifer is still unable to find a suitable body, and in his suffering, his attachment to material things grows stronger. However, in the midst of this all, a being that is "the universe itself" incarnates in a certain test subject.

After his incarnation, Rinka absorbed knowledge, recognizing himself as the Demon God Satan.

Yuri heads to Satan, who has holed himself up in Section 13. Satan accepts Yuri and chooses to live with her. To live together, he decides to abandon Section 13, informing his followers of his withdrawal. As Yuri prepares for their escape, she reunites with Jenny, who is working in Section 13. Upon learning about Satan and Yuri's plan to escape, Jenny plots to free the test subject children at the facility, but...

A newborn Rin, covered in blue flames, attacked the surrounding exorcists one after another. Rin, shaken by the sight and on the verge of being overtaken by his demonic self, is sent to a certain place in the present by Mephisto. Meanwhile, Yukio, who has left the Knights of the True Cross, and Shima arrive at the Illuminati's aerial fortress, the Dominus Liminis. Accompanied by the executive in charge, Homare Todo, Yukio meets Lucifer. Simultaneously, someone from the Grigori Sedes comes to visit Shiemi.

Shiemi cheers up after Rin suddenly appears before her. After hearing Shiemi's voice, Rin regains consciousness and heads back to the past to see the events all the way through. In the past, Satan's possessed body progressively deteriorates, beginning to break down and go out of control. The Blue Night begins at last. As powerful clergy around the world are engulfed in blue flames one after another, the Myodha Sect in Kyoto, the Three Sages in the Vatican, Shiro and the Knights in the Japan Branch struggle against the dire situation.

Using the Koma Sword, Shiro successfully seals Rin's demon heart. This separates Rin from his demonic nature and returns him to Yuri's arms. However, the respite is short-lived as Satan forcibly possesses the body of the Paladin Abel. Satan's love for Yuri has turned into obsession, but Yuri's words can no longer reach him. Satan explodes with emotions and attempts to take possession of Shiro's body. Shiro makes a bold move to prevent himself from being possessed, but...

Shiro and Yuri defeat Satan and escape the clutches of the Knights of the True Cross. However, Yuri's exhaustion catches up to her as she gives her final words to Rin and Yukio and leaves this world. Adding insult to injury, Shiro, overcome with remorse and losing the will to live, is attacked by a demon. Meanwhile, with Satan having disappeared from Assiah, Lucifer despairs of the future research into clones for possession. Mephisto and Shemihaza work to stop Lucifer's rampaging attempt to reduce everything to nothingness.

Shiro offers to leave the twins with Mephisto under the assumption that he has a plan to raise Satan’s children.

Remembering Yuri's words, Shiro relies on Misumi, Nagatomo and the others as he begins raising Rin and Yukio at the monastery. To Yukio, frightened by demons, he guides on the path to becoming an exorcist. To Rin, unable to control his strength, he teaches how to cook and use his strength for kindness. Eventually, the twins become junior high school students, but Shiro, who Satan was constantly targeting, begins to hear Satan's voice more and more each day. And then, that fateful day arrives...