Tokyo, 1991. The first Holy Grail War is about to begin in the city, a secret ritual where seven mages, known as Masters, summon seven heroic spirits, called Servants, to battle for the Holy Grail, a legendary artifact capable of granting any wish. At the center of this conflict is Manaka Sajyou, a young and extraordinarily gifted mage barely in her teens. She is the holder of the highest Master rank, Seraphim, and her summoned Servant is the noble King of Knights, Saber, whose true identity is Arthur Pendragon. For the normally emotionless Manaka, who has been connected to the root of all magic since birth, Saber becomes the fairy-tale prince of her dreams, and she becomes instantly and obsessively devoted to him.

The narrative unfolds from the fragmented perspectives of the various Masters and Servants involved in the war. These participants include Tatsumi Kitano, an ordinary boy who accidentally becomes the Master of Berserker, a scientist whose Noble Phantasm is a miracle drug. There is also the professional camerawoman Elsa Seijou, Master of a loyal Archer from the Middle East; Nigel Sayward, a mage from the Clock Tower who commands the beautiful Lancer; Shizuri Isemi, an unorthodox magus who summons the powerful Egyptian Pharaoh Ozymandias as Rider; the head of the Reiroukan family, Master of the alchemist Caster; and Seiji Jinga, the arrogant Master of the poisonous Assassin.

As the war escalates across Tokyo, from the districts of Setagaya to the bay, Manaka's overwhelming power and connection to the Root make her a nearly unstoppable force. She effortlessly acquires new Servants, like Assassin, who pledges loyalty to her after finding her immune to her deadly poison. While most participants fight for the Grail, Manaka has her own agenda: to use the Grail to grant Saber's wish of saving his homeland, no matter the cost. Her actions grow increasingly dark and manipulative, including planting a deadly curse on the young mage Misaya Reiroukan and sacrificing innocents to awaken a monstrous "Beast" that threatens to destroy the foundation of human history.

As the battles conclude and only a few Servants remain, the full scope of Manaka's terrifying plan is revealed. She intends to use her own younger sister, Ayaka, as the final sacrifice to the Beast. Their father, Hiroki, tries to intervene but is killed by Manaka. In the climax, Saber is forced to confront the monstrous nature of his Master, the girl who claims to love him. Choosing to save Tokyo and honor his own chivalric code, he drives his sacred sword through Manaka's heart, stopping her apocalypse and bringing the first, brutal Holy Grail War to a tragic end.