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.

Awakening her dormant abilities as a devil one day, Yuuko Yoshida aka Shadow Mistress Yuuko, is entrusted with the mission to defeat the Light clan's shrine maiden, a magical girl, by her ancestor Lilith. Yuuko meets magical girl Momo Chiyoda through her classmate Anri Sada, and challenges her to a duel, but loses quickly due to her lack of strength.

Since then, Yuuko has struggled with her role as a devil and her duel with Momo, and borrowed help from her regularly. However, by a strange coincidence, Yuuko also weakens Momo by taking away her power to cooperate in protecting the peace of Tama city.

Mizuki Hijiri, is a high school girl who just transferred schools. At her new school, she has a fateful encounter with boys suffering from chuunibyou (adolescent delusions of grandeur). There is Noda who dreams of becoming a hero, the tragically handsome otaku Takashima who only likes 2D girls, Nakamura the supposedly "reincarnated" angel or devil (he can't decide which), and the self-professed string-puller Tsukumo.

After dreaming about an anime she used to watch as a child, Minoa Asagaya could not forget a particularly memorable scene. However, despite her best efforts, she cannot recall the name of the show. Due to this, Minoa asks for help from her fellow classmates at Sakaneko High School. Her conversation is overheard by Arisu Kamiigusa, the most popular and wealthy girl in class who is also a hardcore otaku. Yet even with her vast knowledge, Arisu does not recognize the show.

After discovering that there isn't an anime club at their school, Minoa and Arisu create the Anime Research Club, as they may obtain the answer to Minoa's mystery if they gather people who share the same interest. Thus, Minoa is exposed to a bizarre new world—the world of anime!

Minoa Asagaya est une nouvelle élève au lycée privé Sakaneko. Bien qu'elle soit une novice en la matière, sa camarade de classe Arisu Kamiigusa l'invite à rejoindre un club de recherche sur les animes. En le rejoignant et en discutant avec les autres membres, elle s'intéressera de plus en plus à cet univers. Cependant, elles sont actuellement en conflit avec le conseil des étudiants qui veut fermer le club.

Pendant ce temps, personne ne se doute que la fin du monde est proche...

Cette troisième saison va couvrir les événements allant jusqu'à 17e tome du roman, à savoir la fin de l'arc Seisen (Guerre Sainte / Holy War).