Unlike his twin brother, Yukio, Rin Okumura never wished to know about their parents and the circumstances surrounding his own birth. Yet the master of time, Mephisto Pheles, gives Rin a key that transports him 40 years into the past when his late mother, Yuri Frederick Egin, was merely a child. With Mephisto's guidance, Rin leaps through the years of Yuri's childhood and her adolescence as an exorcist-in-training. Early on, Yuri meets Shirou Fujimoto, Rin and Yukio's adoptive father. As Rin follows Yuri and Shirou's lives, he witnesses firsthand the initial appearances of Satan, his true father, and the horrors unfolding at the True Cross Order's special Section 13. Yuri's unique connection to Satan eventually leads Rin to the truth behind the most horrific event in exorcist history and the day he and Yukio were born—the Blue Night.

Ao no Exorcist: Yosuga-hen was released on Blu-ray and DVD in two volumes from April 23, 2025, to May 28, 2025.