Enticed by its rumored wealth, Cid Kagenou happily tags along with his sister, Claire, on a trip to the infamous Lawless City. The region is ruled by three monarchs: Yukime, the Spirit Fox; Juggernaut, the Tyrant; and Elisabeth, a dormant progenitor vampire known as the Blood Queen. Hunting Elisabeth down serves as the perfect opportunity for Claire to prove her true mettle. On the other hand, Cid has different objectives—sneaking away from Claire's sight, collecting as much loot as possible, and making Shadow's glorious entrance at the perfect moment.

As Elisabeth's awakening draws near, her subordinate Crimson enacts a treacherous plot, sending the town into a frenzy. Searching for her now-missing brother, Claire finds an unexpected ally in Mary, a vampire hunter, and the pair hurry to the Crimson Tower—the home of the Blood Queen. Meanwhile, Beta and a small team of Shadow Garden recruits also arrive at the Lawless City. As the key players converge on the Crimson Tower, the stage is set for a grand confrontation under the crimson moon.

Kage no Jitsuryokusha ni Naritakute! 2nd Season was released on Blu-ray and DVD in three volumes by Kadokawa from January 24, 2024, to March 27, 2024. It adapts content from volumes 3 and 4 of the light novel.