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Kojou Akatsuki's days as an ordinary high school student in the Demon District of Itogami Island come to an abrupt end after a fateful encounter leaves him with the remarkable abilities of a vampire. It isn't long before he is thrust into the center of attention when it is discovered that he is the fourth primogenitor, an immensely powerful vampire whom most consider to be merely a legend. Fearing Kojou's destructive potential, the Lion King Organization sends in an apprentice sword-shaman, Yukina Himeragi, to monitor, and should he become a threat, kill the boy deemed the world's most powerful vampire. Forced together by circumstance, the two form an unlikely alliance as Kojou comes to terms with his abilities and they both struggle to protect the city from various emerging chaotic forces.
Itogami Island is a manmade island in the middle of the Pacific Ocean where summer never ends. A high school student at Saikai Academy, Akatsuki Kojou, is on his way home from studying with his classmates, Aiba Asagi and Yaze Motoki, when he notices a girl in the Saikai Academy middle school uniform following him.
Yukina moves into the room next to Kojou's. When Kojou sees that she only has a bare minimum of furniture and necessities, he takes her to a hardware store. Kojou's younger sister Nagisa also insists on hosting a welcome party for Yukina, adding up to a very lively day.
The morning after the battle against the Combat Deacon and his homunculus, the town is left in ruins. Yukina had been shocked to see how vastly Kojou's power exceeded that of the Familiar, but now she learns that Kojou can't even control his own Familiars. Kojou and Yukina pursue the escaped Eustach and Astarte to an abandoned laboratory, where another intense battle awaits them...
Eustach and Astarte continue their assault, finally launching an attack on the central support of the manmade island. When Kojou learns that Asagi is trapped inside, he's eager to save her, but his inability to control his own Familiars holds him in place. Unable to see him go on like this, Yukina makes a suggestion he never expected...
It's nearly time for the Saikai Academy ball sports tournament, and Yukina and Nagisa are all fired up to act as cheerleaders! And thanks to the workings of Motoki and Rin, Kojou and Asagi are paired up to participate in the badminton doubles match for their class. Meanwhile, Natsuki is occupied with the capture of some therianthropes that have appeared in the warehouse district, and someone is targeting the Fourth Progenitor again...
Kojou and Yukina meet Dimitrie Vatler, a nobleman who shows an abnormal degree of affection toward the Fourth Progenitor, and Kirasaka Sayaka, Yukina's old friend also under the employ of the Lion King Organization. When Vatler proposes that Kojou capture some terrorists hiding out on Itogami Island and Yukina volunteers to take care of them instead, Vatler challenges Yukina to test her suitability for the task. And, though Sayaka has always been a friend of Yukina's since childhood, her behavior starts to change...
In her excessive defense of Yukina, Sayaka launches an attack on Kojou, but he can't control his powers. Yukina's arrival prevents the situation from growing dire, but Yukina leaves them both on the school roof to think about what they've done.
Gardos the terrorist has reawakened the ancient weapon, Nalakuvera. Kojou and Sayaka barely escape with their lives, but they fall into the depths of the manmade island. Asagi hurries to analyze and control Nalakuvera while Yukina fights a fierce battle to stop Gardos.
The trouble with the Black Death Emperor Faction has been resolved. Kojou has returned to his daily life with Sayaka as a new acquaintance, but he can't decide whether or not he should reveal his vampiric nature to Asagi. It's around that time when he meets a friend of Nagisa's, Kanase Kanon, known as the middle school saint.
Kojou and Yukina prepare to ambush Possession Mask, the group responsible for the attacks around Itogami Island... but one of the Possession Mask members they see is Kanase Kanon.
The deserted island turns out to be a research facility owned by Magus Craft where Kanon's father, Kensei, conducts research. Kojou and Yukina are attacked by a vanguard force, but the one to save them from danger is Princess La Folia of Aldeigia, a young woman with deep connections to both Kanon and Kojou.
When Kojou is disabled in the battle with Kanon, Yukina retreats with him behind La Folia's barrier. Both Yukina and La Folia share their blood with Kojou to aid in his recovery and the awakening of a new power. They have no choice but to rush to Kanon's rescue as her ego slips beyond control and she loses her grip on her humanity.
Itogami Island's tourist industry flourishes as the season of the annual Halloween Fest draws near. Kojou reunites with his childhood friend Tokoyogi Yuuma for the first time in four years, but Yukina and Asagi are not pleased to see the intimate friendship she shares with him. Meanwhile, when the Meyer Sisters suddenly appear at the Keystone Gate, the "witch of the void," Natsuki, finds herself in danger...
Still stuck in Yuuma's body after the mind switch, Kojou rushes to see Yukina and the other girls. At first they're unsure whether to believe him, but after an explanation, Kojou and Yukina try to locate Yuuma in Kojou's body as they draw closer to unraveling the mystery of the witch of the void.
Yuuma's goal was to use the Fourth Progenitor's magic power to free her mother from the prison barrier. In accordance with her plans, the prison barrier appears above the ocean's surface near Itogami Island.
Kojou comes out of the battle with his own body back, but both Yuuma and Natsuki have fallen. The true prison barrier has been revealed along with Yuuma's mother, Tokoyogi Aya, and the other magic criminals who were incarcerated within.
Kojou and company search for Natsuki, whose spiritual powers were stolen by Aya's grimoire and is now missing. Just then, Yukina's surprised voice directs the others' attention to the TV, where Asagi is seen on the live broadcast of the Halloween Fest...
Kojou and Asagi take Sana on board Vatler's boat, the Oceanus Grave II, to protect her from danger. But Kojou's relief is short-lived as he is soon accosted by Vatler's beautiful young maids, and his stimulation is pushed very close to the limit when he ends up sharing a bath with Asagi...
Through Sana, Yukina sees a memory of Natsuki and Aya ten years ago, and then dreams of a happier world she shares with Kojou, Sayaka, and their friends.
Yukina and the other middle school girls are preparing to embark on Saikai Academy's traditional training camp. Yukina is worried about leaving Kojou as she has been released from her observer duties for the trip's duration, but Kojou tells her with a smile to go enjoy her time off.
Asagi has been caught up in Kou's attack. Kojou and Yukina rush to save her, deciding to take her to Mimori's lab for treatment... but when they stop at Kojou's place on the way, another personality takes over Asagi's body.
In his quest to resurrect Wiseman, Amatsuka has finally launched an attack on the ferry carrying Yukina and her classmates. Kanon, believing the others will be safe if she's gone, confronts Amatsuka and tells the sad story of what happened at the monastery five years ago.
"Goodbye, Himeragi..." After hearing Kojou say this to her in a dream, Yukina begins to contemplate her future and the coming of the day when she may have to leave Kojou's side.
Shortly after Yukina lost the use of Schneesturm Wolfin and received an order to return to the Lion King Organization, Itogami Island begins to fall apart under attacks from a magical beast that consumes dragon veins.
Blue Elysium, a new fantasy marine resort, is holding its trial opening and Motoki wants the gang there. Kojo and Asagi end up working a yakisoba booth while Yukina and Nagisa see the sights. Elsewhere on the grounds, Sayaka rescues Yume Eguchi, a younger girl abductee but after giving the girl a photo of Kojo and sending her ahead to the lifeguard centre, is herself taken prisoner by a mysterious sword shaman
Kiriha Kisaki, who works for the Taishikyoku, an agency similar to and in competition with the Lion Kings, offers to release Sayaka once her mission is complete. Until then Sayaka will be put to work. Kojo discovers that Yume is a succubus demon, and her ostensible sister Riru is actually her own alter ego, concocted to cope with past trauma. The others all rise under her mischievous control and make advances upon Kojo.
While Asagi investigates, she is interrupted by Lydianne Didier, who reveals that she is working for the Taishikyoku, managing the LYL program and will protect their systems against all comers. She challenges Asagi to hacking combat and begins her attack. Lilith's spirit awakens early and automatically, contrary to Kazuomi's schemes.
Yukina stalks Kojo as he plays with Yume. A stranger approaches and while chatting her up, half-jokingly accuses her of stalking. He is Gajou, the father of Kojo and Nagisa. Soon after, he leaves the island with Nagisa. On New Year's Eve, Yukina exploits Nagisa's absence to play house with Kojo in his apartment. Motoki arrives with Yume, Kanon, Astarte and Asagi and all visit the temple together. A cryptic message from Nagisa arrives with only a photo of a magic circle in the sky.
Natsuki magically prevents Kojo from leaving her premises. Kanon recruits Nina to spring him. Outside, Kiriha offers Yukina and him a private jet and false travel documents. Her agency is having fun at the expense of the rival Lion Kings. Asagi continues her efforts to leave the island with Mogwai's aid. Lydianne assists, and later the convict Meiga.
Gajou and Nagisa arrive at the temple at Lake Kannawa. He is captured and his jailers are two Lion King miko, Yuiri Haba and Shio Hikawa. Plans for dealing with the sealing relic known as 'Avalon' are discussed. Shirona Kuraki of the Lion Kings will conduct the ritual involving Nagisa, supported by Yuiri. A side-effect of the ritual will permanently expunge the remnant of Avrora from Nagisa.
Myriad forces continue to converge on the frozen Lake Kannawa. Asagi and Lydianne, riding in the pink tank, are joined by Ibliss, a high-ranking vampire from the Warlord's domain, after he rescued them from flying demons. Gajou and Shio carry the comatose Nagisa across the frozen lake, seeking a haven for her.
Shio defies Azama. From afar, Shirona incapacitates the lower level cultists. Okiyama appears on a wyvern and leading a second one to retrieve Azama and they flee. Azama joins the other confrontation and first betrays Ueyanagi, transforming him into a golem, and then attacking Yuiri, triggering a distraught Glenda to transform and fly off with Yuiri, Kojo and Yukina.
Strange occurrences at sea result in Itogami Island becoming isolated. Nagisa continues to suffer effects from her previous exertions. A terrorist group known as Tartarus Lapse begins operations on the island.
The terrorists launch an attack upon the warehouse district. Afterward, Kojo and Himeragi meet the terrorist leader, Senga Takehito, who tries to recruit them. He reveals his beliefs about the true nature of the island, its purpose of reviving Cain, and his plans to oppose this.
At Mogwai’s urging and with Motoki’s assistance, Asagi makes her way to the Keystone Gate in order to end the hacking attack upon the island’s network. Meanwhile, Kojo and Himeragi battle ineffectively against the demons unleashed by the terrorists.
After the terrorist incident on Itogami Island, Kojo and the others are helping with the Island's recovery. On the other hand, Asagi, who gained popularity with the public for preventing hacking in the past incident, works as an ambassador for revival activities for the Island Management Corporation. However, Kojo feels like something is off when he sees Asagi on the big screen.
Kojo and the others go to rescue Asagi, who was imprisoned on the 0th floor of the Keystone Gate. Kojo is worried about Himeragi's poor condition, but Himeragi goes with Kojo nonetheless. What was waiting for Kojo and Himeragi on the 0th floor?
Kojo and the others are helpless by the power of Meiga Itogami's Cleansing ability. Kojo wonders what the hell this Cleansing ability is. At that time, the truth about the Cleansing is passed on to Kojo. Will Kojo be able to protect Himeragi and Itogami Island from Meigawa Itogami?!
Itogami Island had returned to a peaceful state and Kojo's party was getting excited about the upcoming Valentine's Day. Meanwhile, Kojo sees Asagi getting into a car with one of Vatler's subordinates, and starts to get suspicious. Grenda, who was with Shio and Yuiri, is attacked by Veres Aladar, the Imperial Council Chairman of the Warlord's Empire. Grenda flees to Itogami Island, where Kojo is located.
Kojo goes to Iblisveil Aziz in search of answers on how to defeat Veres Aladar, but Iblisveil only gives Kojo a vague answer. Kojo returns to the agreed place of the duel shorthanded and begins the duel.
Kojo wakes up at Natsuki Minamiya's house. On TV, Asagi and Vatler appear to be working together and declares war against the Holy Ground Treaty Organization. In addition, Asagi says that Grenda will use Cain's legacy that she has protected as her power, to help save Itogami Island. Meanwhile, to save Nagisa, whose life is in danger, Hektos tells Kojo and the others that she will need to hold a ceremony.
With the help of La Foria and Veres Aladar, Kojo broke into the council and declared Itogami Island as his territory as the 4th Primogenitor and gained the right to veto the attack. But for him to be recognized for this, he must expel Vatler from the island and become a true ruler. Can Kojo defeat Vatler, who has absorbed the power of the Cleansing, and save Itogami Island from the crisis?!
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