The game takes place half a year after the events of the first game, prior to the events of the second game. Komaru Naegi, the younger sister of the first game's protagonist, Makoto Naegi, has spent the past year locked inside an apartment complex in Towa City, unaware of the events that have gone on in the outside world. She is suddenly forced to flee when she was attacked by deadly Monokuma robots and comes across Future Foundation member Byakuya Togami, who gives Komaru a special Hacking Gun that can fight against the robot and orders her to escape the city. However, Komaru's escape fails and she is captured by a group of elementary-school children known as the Warriors of Hope, who seek to create a utopia for children by murdering all the adults with their robots. They force Komaru to join their "Demon Hunting" game and drop her into the city, where she is saved by Homicidal maniac Genocide Jack, who soon reverts to her true self, Toko Fukawa, a survivor of Hopes Peak High School's killing game. Toko can now control Jack through the use of a stun gun. Learning that Byakuya may have been kidnapped by the Warriors of Hope, Toko agrees to team up with Komaru to find Byakuya and escape the city. Along the way they encounter a resistance group, run by Haiji Towa, and meet a white bear robot named Shirokuma.
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