The story revolves around Rin Okumura, who, along with his younger twin Yukio Okumura, was raised by Father Shiro Fujimoto, an Exorcist. One day, Rin learns that he and Yukio are the sons of Satan. Witnessing Shiro dying to protect him, Rin draws the demon-slaying sword Kurikara (倶利伽羅), which restrains his demonic powers. From that moment on, Rin not only gains demonic features like fangs and a tail, but also the power to ignite into blue flames that destroy almost anything he touches.
Rin wishes to become an Exorcist like his guardian to become stronger and to defeat Satan. He enrolls at the prestigious True Cross Academy (正十字学園, Sei Jūji Gakuen), an exorcist cram school, which is actually the Japanese branch of the True Cross Order (正十字騎士團), an international organization dedicated to protect Assiah (human realm) from the Gehenna (demonic realm). Much to his surprise, Rin finds that Yukio is already a veteran Exorcist and is one of his teachers. Thus begins Rin's journey to become an Exorcist, accompanied by his brother and his fellow students who quickly become his close friends.