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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...