In the waning days of February, with entrance exams finished and graduation drawing near, the students of Kunugigaoka Junior High School's Class 3-E find themselves under the government's ever-watchful eye as the deadline to assassinate their teacher approaches. During this tense waiting period, the class takes time to reflect on the unforgettable year spent with their tentacled instructor, Koro-sensei. Their memories unlock a collection of untold stories from their daily lives—moments that were never depicted in the original television anime. These recollections include the talented Sugaya displaying his artistic side in Art Time, Maehara stepping up during Retaliation Time, special swimming lessons, unexpected Valentine's Day chocolates, and confrontations with the main campus's elite Class A.

The central narrative also expands beyond the classroom during winter vacation, when Koro-sensei becomes the target of four assassins. Though he easily evades their attacks, his subsequent visit to their local izakaya leads him to save the blind owner Azusa and her daughter Hotaru from a deadly incident, reaffirming his determination to fulfill his duty as a teacher until the very end. Meanwhile, the students of Class 3-E continue their relentless attempts to kill their Mach 20-speed teacher, who responds with a smile while praising their growth and skill. As the film moves toward its conclusion, a graduation album reveals fleeting glimpses of the students' futures, bringing the saga of Class 3-E to its heartfelt and final closure.

The main cast includes Jun Fukuyama as the voice of Koro-sensei, the powerful yellow octopus-like creature who is both the students' beloved homeroom teacher and their assigned target. Mai Fuchigami returns as the observant and talented Nagisa Shiota, while Nobuhiko Okamoto voices the rebellious genius Karma Akabane. Aya Suzaki plays Kaede Kayano, and Tomokazu Sugita reprises his role as the stoic government agent Tadaomi Karasuma. The film also introduces new characters, with Kikuko Inoue as Azusa, Sayumi Suzushiro as Kaho Tsuchiya, and Mai Kanazawa as Kokona Tagawa.