Rin Okumura, a boy aiming to become an exorcist yet born the illegitimate son of the demon god Satan, advises his classmate Sei Godaiin, who begins to see demons. Despite Rin asking Ryuji Suguro and the other Exwires attending the Exorcism Cram School for a way to make demons invisible, he is unable to find a solution. Meanwhile, Rin is invited to dinner by Mephisto Pheles, the Preceptor of the Japan Branch of the Knights of the True Cross and director of the True Cross Academy. However...

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.

After his secret is exposed, Rin takes part in a special mission along Shura and Yukio to retrieve the "Left Eye of the Impure King", a demon relic that was stolen from the True Cross Academy's vault. In the occasion, they fail to retrieve it, but discover that the culprit is Saburota Todo, one of the exorcists in charge of the vault that was corrupted upon being possessed by a demon. After hearing that there was an attempt to steal the Left Eye's sister relic, the "Right Eye of the Impure King" in Kyoto, the Order sends a team there to investigate, including Shura, Yukio and the Exwires, who are in conflict after learning the truth about Rin.

The Exwires arrive at Kyoto, and Ryuji, Konekomaru and Renzo take the opportunity to reunite with their families, while Rin and the others tend to the Exorcists of the Myoda Sect, who got wounded guarding the Right Eye of the Impure King. In the occasion, Rin meets Ryuji's father, and learns that Ryuji is resentful of him, as despite being the leader of the Myoda Sect, he is not respected by the others, as he relegated his duties since the Sect, which was weakened after losing several of its members on the Blue Night, joined the True Cross Order. Meanwhile, Todo, with the Left Eye of the Impure King replacing his own, contacts his mole inside the Sect, planning another attempt to steal the Right Eye.

Who is betraying the Myoda sect? Without high priest Tatsuma in attendance, the general meeting falls into chaos and ends without a conclusion. As Suguro resolves to find and question his father, he witnesses someone sneaking into the Kyoto field office…

Although the traitor was revealed, the Right Eye of the Impure King has been stolen. While confronting Ryuji, Rin loses control of his blue flames in front of the gathered exorcists. In all of the commotion, Tatsuma slips Shura a letter addressed to Rin.

Miasma spreads through the streets as the exorcists begin to counter the Impure King’s growth. Rin leaves with the other students to find Tatsuma. Yukio is on the front lines, unaware his brother has left his cell, when he notices something strange…

The sporangium has finally burst, revealing the Impure King. Assaulted by the miasma, Suguro barely maintains the barrier. And every passing moment brings him closer to his limit. Rin questions why he can’t draw his sword, even when backed into a corner.

Rin finally manages to draw the demon sword. Shura tells him to, “Win a place for yourself in this world!” However, there doesn’t seem to be a way to stop the Impure King’s overwhelming growth. And if Suguro’s strength fails, the barrier will collapse!

The sight of a blue flame burning in the night sky is reminiscent of “Blue Night,” but has brought about a completely different result. Now that the incidents relating to the Impure King have been concluded, those affected are moving on.

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…

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...

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.

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...

The Myoda Sect has an emergency meeting to discuss the failed attempt to steal the Right Eye of the Impure King and discover who among them is the traitor collaborating with Todo. In the occasion, suspicions were raised towards two of the sect's exorcists, Renzo's older brother Juzo and Mamushi as they were present at the scene and were Todo's students in the past, but the head priest, who did not attend the meeting, was counted as a suspect as well, much to Ryuji's anger. Meanwhile, Rin continues with his training to control his flames while trying to reconcile with his friends, who fear how the Myoda will respond once they learn that he is the son of Satan.

Shiro Fujimoto, Rin and Yukio’s adopted father, encountered Tatsuma Suguro while trying to take the demonic sword, Kurikara. Tatsuma’s letter reveals the circumstances of how the sword, which is the Myoda Sect’s main object of worship, came to Rin.

The Impure King has been revived! In his letter, Tatsuma asks Rin to use the Koma sword to fight, but will that even be possible? And to make matters worse, Mephisto suddenly appears with the news that Rin has been sentenced to death!

“You despise your brother, don’t you?” Yukio is shaken as Todo tells him to admit his true feelings. Yukio reflects on the thoughts he’s had since an early age. Meanwhile, Suguro has inherited the Gouha-en, and with it, he and Rin head to the sporangium.

Yukio Okumura, Rin's younger twin brother and Intermediate Exorcist First Class, is summoned to a high-level inquiry meeting of the True Cross Order to be questioned about Saburota Todo, the mastermind behind the resurrection of the Impure King. Suspicious of the imposing atmosphere, Yukio recalls the words of his late adoptive father, Shiro Fujimoto. Meanwhile, the Exwires are tasked with exorcising "Mayuko of the Toilet." However, Izumo Kamiki holds a certain grudge against Shiemi Moriyama.

Arthur A. Angel and Lightning capture a spy hiding among the Knights of the True Cross and learn that the secret society, the Illuminati, is planning to abduct someone for a certain project. And now, the time for their plan is at hand. After hearing the news, Shura Kirigakure gathers the Exwires. Meanwhile, Izumo confronts Takara and angrily explodes when she sees a particular stuffed animal in his hands...