20 years have passed since the climactic events of RWBY: Death Blossom, the war of Vacuo, and the Multiversal Convergence. The world has changed, and the forces of good and evil have realigned. The protectors of Seir, the GUARDIANS, led by Yang Xiao-Long, now known as Solaria Prima, vigilantly protect their new home and the entire Multiverse. The Deathsinger, Ruby Reaper-Rose, and her Reaper's Zodiac have sworn vengeance and domination, their eyes set on a new conquest-The Entire Multiverse itself. With newly forged alliances and powerful dark magic at their disposal, the Zodiac seeks to capture the "Crescent-Spark," a mysterious child born during the Convergence. This child holds the key to unlocking the prison of Galbatorix, promising untold chaos and darkness. The next generation, the children of the original protagonists, step into the limelight. Enrolled in the New Hunter-Knight Academies, they are trained to become the defenders of the future. These academies, protected sanctuaries during the war, are not exempt from danger. Forces of The Zodiac, led by Ruby's own daughters, infiltrate and threaten the sanctity of these academies, putting young heroes to the test.

It's been three years since anyone has heard from the CPU's or the Oracles. In that time, Gamindustri has fallen to total chaos. The CPU candidates have lost their ability to transform due to the sudden lack of shares. People have started walking around limp and with white in their eyes due to everyone fighting for food. Nepgear has decided she has had enough of this torture. She wants to find her sister and the three other CPU's, but she can't do it alone. Desperate for aid, she runs as fast as she can towards Lastation's Basilicom, avoiding raiders and hostiles along the way. But what she found inside isn't what she expected to find at all. Nepgear finds out the hard way that some people fall into the chaos and turn to insanity quickly. Barely managing to escape from the grip of death, she returns to her hideout. She has a choice to make. Try and get Rom and Ram's help or go out into the wasteland alone to search for Neptune. Sometimes, the hardest choice is the right choice but...all it takes is the will of a single man.