Momiji Fujimiya is a 15-year-old school-girl who discovers that she is the hereditary Princess Kushinada. She joins the TAC, a secret government force unit in charge of battling the Aragami, a group of unnatural beings that have awakened from legend and are attacking Japan. Momiji struggles to come to terms with her new status as the Kushinada princess in the midst of finding her role in the TAC force, and trying to make sense of her yet to be defined feelings towards her protector Kusanagi.

Momiji wakes up in the middle of the night to find she's now in Tokyo. The next morning, she reads a letter from her Grandma explaining her responsibility as the Kushinada. Momiji gets upset when told that the TAC (Terrestrial Administration Center, the government's special force group) will protect her and she is now under the custody of TAC chief Mr. Kunakida. Momiji thinks she's been sold to slavery and tries to escape, only to run into Kusanagi, who tells her to keep the glowing "blue seed" on her chest a secret. This seed, Momiji discovers later, empowers her psychically and helps her detect Aragami, which comes in handy later when alone at TAC headquarters and facing a nasty crow-like Aragami.

On a patrolling assignment together, Momiji only angers Kome with her attempts at being pleasing. Kome brushes off their duties to go gambling and gun shopping. Momiji senses Arigami with her blue chest seed and directs Kome where to find it. Kome fails at trying to blow off the Arigami's head, and Kusanagi enters to kill the Arigami by destroying its own blue seed. All in a day's work.

Kusanagi threatens TAC's biotechnology specialist and workoholic Ms. Matsudaira, as well as her son, when she announces she wants to run tests on Momiji. Momiji is frightened about being tested but is angered by Kusanagi's behavior. While she confronts Kusangi, they both are attacked by an Aragami jellyfish. Ms. Matsudaira shows up in her helicopter and kills the Aragami, saving both Momiji and Kusanagi.

Yaegashi, TAC's elite computer analyst, starts to doubt his worth in the group when he is unable to help Kome in an Aragami attack. Momiji eventually kills the monster and later tries to console Yaegashi. Momiji expresses interest in Yaegashi's computer programming and visits his house to see his new probability determination program, which she discovers Yaegashi tests out by determining the kind of underwear she is wearing. Momiji leaves upset and, on her way home, she is confronted by an Aragami. Yaegashi catches up with her and uses his program to conquer the monster and save Momiji.

Momiji is determined to help rescue a kidnapped girl whose father was one of the scientists that studied Momiji's sister, Kaede, and was part of the Kushinada Project that started years ago. The Aragami want the father to disclose valuable information about the Kushinada, which they'll use as protection against Momiji and her powers. In her quest to save the girl, Momiji ends up confronting Miahara, the Congressman at a castle in an amusement park. The TAC team and Kusanagi save Momiji with the hidden tracking device they planted on her earlier.

Momiji starts having romantic dreams about Kusanagi and starts to question her true feelings towards him. The ostentatious Sakura shows up in the episode just in time to rival Momiji in an idol singer contest. Sakura, with Kusanagi's help, saved Momiji from an Aragami skirmish while on her way to the contest and afterwards boldly flirts with Kusanagi. During the contest, Momiji doesn't back down from Sakura when they end up on stage together. Another Aragami attack ensues and Momiji saves the day by sympathizing with the monster.

Aragami dogs are roaming the streets, and the TAC team is having a difficult time stopping the pack. Dogs are winding up dead though, and the team doesn't know who's responsible for killing them. Meanwhile, Kusanagi questions Momiji on what she believes to be a date. She finds out later that she misunderstood his invitation to go out and his intentions were only to hunt the Aragami dogs and Mimiji's mitama. When a rabid dog confronts the two, a strange man called Murakumo appears, kills the pooch with one blow, and then disappears.

An Aragami frog terrorizes the Tokyo subway system and Momiji takes it upon herself to follow the frog until it leads her to a shine. Murakumo, the strange man from the previous episode, is there and when the floor falls from under Momiji, Murakumo watches and laughs. Kusanagi finds Momiji lying still and gives her mouth-to-mouth to revive her. Momiji mistakes the CPR as a kiss and starts to obsess over her feelings towards Kusanagi. Meanwhile, Kusanagi confronts Murakumo but turns out to be no match for the man with more mitama. This time Momiji is the one who saves Kusanagi with her powers. She's proud to become aware that her gift is important, but she's confused about her status with Kusanagi.

Momiji is not thrilled when Sakura transfers to her school. The competition between the two girls intensifies, but their rivalry is put on hold to save a group of girls held captive by a swarm of Aragami spiders. When screams echo from the school gym, the two, along with Kusanagi, hunt down and battle the huge mother creature but wind up trapped in its web. Momiji, who thinks she was inferior to the other two because her powers do not match theirs, kills a small spider on the neck of one of her schoolmates. This action drains the power of the larger spider and leaves room for Kusanagi to kill it. The school returns back to normal but the antagonism between Momiji and Sakura intensifies.

Momiji's involvement in the TAC is affecting her schoolwork. She tries to concentrate on her studying, but when a giant centipede shows up in the city, wrapping itself around buildings and shedding its strange, glowing skin, Momiji can't help but to investigate. The blue seeds on her chest give her an ominous feeling and when she follows her instincts, she finds Kusanagi badly wounded after a fight with Murakumo. Kusanagi leaves her in a hurry, and when another centipede shows up the next day and attacks Kusanagi, Momiji discovers that Murakumo controls the creature. Momiji is knocked unconscious by the centipede and is saved by Kusanagi, but the glowing skin left by the monster is a forewarning of immanent danger.

The TAC team is aware of Momiji's romantic feelings towards Kusanagi and Kome calls Momiji out telling her the odd dreams she's been having is because she's in love with Kusanagi. Before Momiji can confront Kusanagi, she is called upon to go into the city's underground. Momiji searches the sewers until she comes across her twin sister Kaede, who is taking care of a baby enclosed in a large mitama. The baby turns out to be Susana-O, the Aragami god. The sighting leaves Momiji confused Kusanagi upset.

Murakumo and Kaede travel through Nara with the baby Susana-O. The infant's mitma buds an Aragami that takes the shape of pollen and begins to kill the people of Nara. Momiji distresses over her current standing with Kusanagi and becomes even more troubled when he expresses concern for Kaede. Momiji deals with her anxiety by pledging that if she kills the new Aragami by herself, Kusanagi will fall in love with her. While battling the monster, Kusanagi prepares to aid Momiji but gets distracted when he senses Kaede. He leaves in search for Kaede, furthering Momiji's torment. Momiji doesn't know it, but Yaegashi has made a similar pledge with the prospect of gaining Momiji's affection.

Reports abound about a legendary sea monster called the Kappa roaming countryside and the TAC team investigates. On their journey, Momiji and Kome meet a girl who used to go to school with Kaede. The girl first mistakes Momiji for Kaede and cannot stop praising her for her kindness, intelligence and overall character. The acclaim raises Momiji to doubt herself. Momiji's anxiety only intensifies when she learns later that Kaede knew Kusanagi watched over her and she had an attraction towards him. Later, numerous Kappas appear and Sakura is charged with fighting them off. Kusanagi arrives just in time to save Sakura from being flattened. The next day, Momiji and the TAC team confront another Kappa. Kusanagi is trapped by the Kappa and Momiji, refusing to listen to his orders to run away, shields him with her own body. The battle ends when the Kappa shifts its attention to a tree being chopped down during a construction project. It melts away as it tries to protect the tree.