As instructed by Totosai, the girls begin to search for Bokuseno to find out where to acquire a Kyuyokon root for Towa. During their search, they come across a village where women with long hair are attacked by a sea snake demon.
Towa, Setsuna, and Moroha continue their search for Bokuseno. Meanwhile, while Sesshomaru and Jaken watch over the sleeping Rin, Jaken recalls the day fourteen years ago when Zero placed a curse on Rin.
The girls arrive at Mount Musubi to retrieve the Kyuyokon root. The mountain is surrounded by a barrier, which Moroha is able to pass through easily due to her spiritual powers. When she enters, she finds a girl sleeping on the mountain.
The girl on Mount Musubi introduces herself as Rion, the daughter of Kirinmaru, who had been sealed on the mountain for 600 years. She asks Towa and the others to defeat her father in order to set her free and put a stop to his plans.
Setsuna is kidnapped by Princess Aiya's servants and is brought to her mansion. Wanting to avoid her studies, Princess Aiya asks Setsuna to switch places with her for one day. When her tutor arrives, however, it turns out to be Hisui.
Takechiyo requests Moroha to be his bodyguard when he needs to return to his home to deal with an ongoing family feud. Meanwhile, Kohaku tries teaching Towa a lesson in running away from battle when he notices her reckless fighting habits.
Setsuna travels with Kohaku, Hisui, and the other demon slayers to a northern village to assist the demons slayers of the north. Meanwhile, Kirinmaru appears before Towa, who is accompanied by Riku and Rion.
The demon-god Mayonaka continues to attack Gokoku Village with Flame Bulls to acquire the village's sacred object. While the demon slayers defend the village, Setsuna meets Mayonaka and learns of his reason for attacking Gokoku Village.
On the new moon, Zero sets her plan into motion, targeting Towa while she's powerless. Setsuna also loses her powers while being hunted by a snow demon. Moroha learns from Hachi about Inuyasha and Kagome's battle against Shogen Mamiana.
While in her human form, Towa is abducted by Zero and Nanahoshi. Moroha, Takechiyo, and Hachi continue their fight against Shogen. Kohaku and the other demon slayers fight off the snow demon that is searching for Setsuna.
Zero uses Nanahoshi's insects to extract Towa's sadness from her, causing Towa to revisit her memories of loneliness as she grew up in the modern age. Meanwhile, Sesshomaru finds Setsuna and orders her to go to the Tree of Ages to see Rin.
An enraged Towa attacks Zero with the intention of killing her. Setsuna arrives to stop Towa because of Rin's curse, which cannot be lifted until Zero moves on from her past regrets. Meanwhile, Sesshomaru gives Moroha the Black Pearl.
Kirinmaru takes the Black Pearl from Moroha and demands that she find Akuru. Sesshomaru, Towa, and Setsuna arrive at the scene and Sesshomaru begins to duel with Kirinmaru. The girls join in the fight, but this rouses Kirinmaru's anger.
Towa, Setsuna, and Moroha are sucked into the Black Pearl and are sent to the border of the afterlife, where Moroha is reunited with Inuyasha and Kagome. Meanwhile, Rin and Jaken search for Towa, whose sword is needed save Sesshomaru.
Inuyasha comes up with a plan to escape the border of the afterlife. At the grave of the Great Dog Demon, Inuyasha instructs Towa to summon Tenseiga, which will be the key to their escape.
After removing Kirinmaru's demonic energy from Sesshomaru, Towa collapses and is in critical condition. Kirinmaru appears before Inuyasha, Kagome, and Moroha. In the Reiwa era, Osamu Kirin sees the Grim Comet approach closer to the earth.
To stop the Grim Comet in the modern era, Towa, Setsuna, and Moroha must travel through time using the Windmill of Time. But to use it, they first must defeat a demon called Meidomaru.
Towa, Setsuna, and Moroha return to the modern age. Osamu Kirin asks for their help to defend the city from the demons that have appeared due to the Grim Comet.
Towa, Setsuna, Moroha, and Osamu Kirin work together to stop the Grim Comet from hitting the earth. Meanwhile, back in the feudal era, Inuyasha and the others fight off the swarms of demons that emerged from the Windmill of Time.
Osamu Kirin brings the Grim Comet into the feudal era. He finds Rion and convinces her to work with him to create a world they both desire. Towa, Setsuna, and Moroha are stuck in the present and must find a way back to the feudal era.
Under the control of Rion and Osamu Kirin, the Grim Butterfly sets out to destroy all of the demons in the world. Towa and the others approach and enter the butterfly to rescue Rion. Meanwhile, Sesshomaru and Kirinmaru begin to battle.
Towa is able to defeat Osamu Kirin, but not without a cost. She rejoins Setsuna and Moroha and assists with cutting Rion's Threads of Fate. Whenever a thread is cut, Rion's true feelings for her father are revealed.
The feudal era is saved from the Degenerate Age. Inuyasha helps repay Moroha's remaining debt. Towa and Setsuna receive kimonos from their mother, Rin. Towa, Setsuna, and Moroha accept a demon-slaying request from a mysterious man.
