Momiji Fujimiya (藤宮 紅葉, Fujimiya Momiji): Momiji is the descendant of the "Kushinada". She lives in Izumo, where Princess Kushinada lived. An eighth-grade student, she was unprepared to understand her destiny to battle the Aragami. She becomes a member of the TAC in order to stop the Aragami from destroying humanity. An ironic twist of fate has Momiji carrying a mitama – an Aragami "soul" – embedded in her chest. At awkward times, Momiji is the recipient of panty shots and jokes about the type of panties she wears. Her relationship with Kusanagi takes a turn for the better during the shielded town incident, where she finally confesses her love for him, and he in turn tells her to wait for him.

Momiji is the primary protagonist of the series. She is the descendant of the "Kushinada" who actually lives in Izumo where Princess Kushinada lived. An eighth-grade student in middle school, she was unprepared to understand her destiny to battle the Aragami. She becomes a member of the T.A.C. in order to stop the Aragami from destroying humanity and the world. An ironic twist of fate has Momiji carrying a mitama—an Aragami "soul"—embedded in her chest. At awkward times, Momiji is the recipient of panty shots and jokes about the type of panties she wears.

In 1992, Momiji Fujimiya is a middle school student living with her mother and grandmother in the city of Izumo, Shimane. One day, she is confronted on her way to school by a cat-eyed man with blue magatama beads embedded in his hands, who attempts to kill her. He refers to her as Kushinada. Momiji is saved by the sudden appearance of two government officials, one of whom shoots the man in the arm and sends him fleeing.

Momiji is intrigued as to why she was referred to as the Kushinada. She discovers that the Kushinada refers to an ancient princess whose blood holds the power to stop the ancient monsters known as Aragami by sending them to an eternal sleep. Momiji dismisses the idea that she could be such a person, but reconsiders after vines begin to appear from every crack and opening attempting to capture her.

Momiji tries to escape, not knowing that the vines are being employed by a powerful Aragami known as the Yamata no Orochi. She is saved by the man with the magatamas embedded into his hands, who introduces himself as Mamoru Kusanagi. He confronts Orochi using Momiji as bait. The plan fails and the government officials appear again. They reveal themselves to be members of the Terrestrial Administration Center (TAC for short), and subdue Orochi. However, with the last of its strength, it attacks Kusanagi.

Momiji saves Kusanagi by taking Orochi's blow. Impaled by the Aragami, instead of dying, she is instead fused with the magatama, more specifically identified as a mitama, which gives Momiji the ability to sense the presence of other Aragami. The TAC agents explain that they are an organization dedicated to defeating the Aragami, who seek to destroy humanity. The current Kushinada, Momiji, must aid them because the other Kushinada, Momiji's twin sister Kaede Kunikida, is now dead. Momiji, wishing to discover more about the twin sister she never knew and also to fulfill her destiny, agrees to join the TAC under the protection of Kusanagi, who wishes to destroy his former masters, the Aragami.

Kusanagi repeatedly attempts to kill Murakumo, a man with eight mitamas who kills any renegade Aragami. Kaede reappears along with a strange energy field in Tokyo. Murakumo and Kaede intend to resurrect the god Susanoo and purify the world of humanity's influences, with Kaede acting as the leader of the movement.

There is also a three episode OVA, Blue Seed Beyond, which takes place two years after the end of the TV series. It concerns what seems to be a resurgence of aragami (actually created via biotechnology), and introduces a new character, Valencia Tachibana. Like Kusanagi, she was implanted with a mitama without turning into a full aragami.