Now that Koyomi Araragi has graduated from high school, his own story has concluded. However, the stories of the girls he once saved from supernatural afflictions are far from over. The narrative shifts its focus to their lives, struggles, and growth in his absence, while also exploring pivotal events from the distant past and Koyomi's own life as a university student.

The setting remains the same peculiar town, but the passage of time is evident. Koyomi is now a first-year student at National Manase University, trying to distance himself from the world of apparitions and enjoy a normal campus life alongside a sharp-tongued new friend named Meniko Hamukai. The primary responsibility of dealing with oddities has largely been entrusted to Yotsugi Ononoki, a tsukumogami (a living doll-like apparition) who has taken up residence in the Araragi household. Her mission is to monitor Koyomi's younger sister, Tsukihi Araragi, who harbors the immortal phoenix within her.

The season, which adapts the Off Season and Monster Season light novels, is structured into several distinct narrative arcs.

The story begins with the Tsukihi Undo arc. Yotsugi is living as a doll in the Araragi home but accidentally reveals her sentience to Tsukihi. This forces Yotsugi into an absurd and comedic struggle to convince Tsukihi she is just an ordinary doll, a task complicated by the phoenix's nature, which causes Tsukihi to forget past traumas and repeat her mistakes endlessly.

Following this, the Nadeko Draw arc centers on Nadeko Sengoku. Once a middle school girl who became a god, Nadeko is now a withdrawn third-year student avoiding school while pursuing her dream of becoming a manga artist. At Yotsugi's suggestion, she uses her powers to create four clones representing different facets of her personality to help her draw faster. However, the clones escape and run rampant, forcing Nadeko to confront her fractured identity and literally battle her past selves to achieve personal growth and reclaim her life.

The narrative then delves into a prequel story set 600 years in the past. The Acerola Bon Appétit arc reveals the origins of Shinobu Oshino, the ruined vampire. It follows a beautiful and lonely princess named Acerola and her fateful, tragic encounter with the immortal and powerful vampire, Deathtopia Virtuoso Suicide-Master, which leads to the creation of Kiss-shot Acerola-orion Heart-under-blade.

Finally, the Shinobu Mustard arc returns to the present. Koyomi is called upon by the enigmatic specialist Izuko Gaen to solve a bizarre case where female students at Naoetsu High School are turning into mummies. The investigation leads him back to his old haunts and directly into a reunion with the legendary vampire Deathtopia, who has awakened from a long slumber. This arc brings together Koyomi, Shinobu, and a host of familiar faces to unravel a mystery tied to the very nature of vampires and the consequences of immortality.

Throughout these interconnected tales, the season explores themes of growing up, identity, and the lasting impact of past choices, all presented through the series signature dense dialogue, visual metaphor, and unconventional storytelling.