Towa Higurashi learns about an incident that took place decades ago involving a half demon named Inuyasha and a priestess named Kagome.
Half-demon twins Towa and Setsuna are separated from each other when a mysterious tunnel sends Towa into the future, where she is found and raised by Kagome Higurashi’s brother Sota.
In the present day, a demon emerges through the Sacred Tree at Higurashi Shrine with Setsuna, Towa’s twin, and the bounty hunter Moroha in tow. Towa, Setsuna, and Moroha struggle to battle the demon, whose powers have been strengthened with two Rainbow Pearls, but seeing Setsuna in trouble awakens Towa’s latent demon powers.
Towa decides to return to the feudal era to help Setsuna regain her memories. The trio enter the corridor leading to the feudal era, but within it awaits the spirit of a certain priestess.
Safely back in the feudal era, Moroha heads to the corpse dealer to claim her bounty. Meanwhile, Towa and Setsuna take on a request to slay Jakotsumaru, a boy who has been extracting bones from humans and beasts in order to revive his father, the demon beast Tokotsu.
Travelers are going missing one after another. Towa, Setsuna, and Moroha head to the northern mountains to crack the case, but instead they find a village completely overrun by ghost cats!
On her way to search for the Dream Butterfly, Towa meets a strange young man named Riku. Towa offers him an apple, and in thanks, Riku presents her with the genuine Kikujumonji sword.
After fleeing from the deputy shogun’s estate, Yotsume borrows the power of a Rainbow Pearl to unleash his Dream Gazing spell upon the Half-Demon Princesses, who are hot on his trail.
Moroha accepts a job to slay Konton, a member of the Four Perils said to have defeated Meioju, a demon beast with the ultimate armored shell.
The Half-Demon Princesses are tasked with slaying Kinka and Ginka, conjoined twins of the Ka Demon Tribe whose battles for dominance have been wreaking havoc everywhere.
Something wicked lurks in the Man-Eating Pond, devouring any human, beast or bird that comes near. Towa and Setsuna meet Hikomaru and Chiyo, siblings who lost their parents to the pond.
The demon Nikosen was a sage before evil consumed his soul. Konton orders him to kill the Half-Demon Princesses. Towa struggles as her demon powers fade and she turns into a human.
When a demon begins to devour virtuous monks and Shinto priests in the region, Hisui is assigned to guard his father, Miroku, who has been undergoing harsh training for the past two years.
Towa and Setsuna set off to slay Homura, an evil mountain god who has abducted a beautiful maiden. The twins learn that Homura was involved in the forest fire that separated them.
The truth behind the night that sealed the fate of Towa, Setsuna, and Moroha’s parents is finally revealed.
Moroha once had a master named Yawaragi, who was keeping a life-threatening secret. In order to resolve the secret and protect her pupil, Yawaragi made an agreement with Jyubei.
Konton devises a plan to destroy the Half-Demon Princesses. Riku offers to help him out. The three girls are lured into a ravine and fall right into Konton’s trap.
Konton learns of the origins of the Rainbow Pearl and the connection between Kirinmaru and the Dream Butterfly. He summons an ogre to attack the Half-Demon Princesses.
The deputy shogun’s daughter Aiya offers to employ the demon slayers if they win in a battle against the bounty hunters.
Setsuna opens up to Towa about the hidden village for half-demons where she was raised for most of her childhood.
On the night of the new moon, Riku pays Towa a visit to chat. Unfortunately, he’s not the only one planning to drop by.
Zero removes the seal that Miroku placed on Setsuna to suppress her demon powers, awakening the latent demon blood within.
Setsuna and Towa hire Moroha to help slay Zero. The trio successfully track Zero down, but Riku stands in their way.
Towa, Setsuna, and Moroha are left to confront Kirinmaru, but in the face of overwhelming power, they must pay a great price.
Sesshomaru hands the broken Tenseiga to a grieving Towa, leaving Setsuna’s fate in her hands. Will Towa be able to bring Setsuna back to life?
Having restored Setsuna to life and recovered from her exhaustion, Towa finds herself alone as Setsuna and Moroha begin searching for the mystical root needed to forge Towa a new sword.
Jaken recalls that fateful day fourteen years ago, when Zero placed a curse on Rin that would make her slowly rot away to an excruciating death. The three girls search for Bokusen-Oh, who may have a lead on the whereabouts of Towa’s new weapon.
The three girls arrive at Mount Musubi but are trapped by a powerful barrier. Moroha manages to escape and runs into something unexpected.
Rion used to travel the world with her father Kirinmaru, but one day, her soul was sealed deep within Mount Musubi. Longing for freedom and peace, Rion asks Setsuna to sever the thread of fate that connects her to her father.
Setsuna is kidnapped by Princess Aiya, daughter of the deputy shogun. Wanting to escape her studies, Princess Aiya begs Setsuna to be her body double for a day, but the princess’s new tutor turns out to be Hisui posing as his older sister Kin’u!
Revealing that he was once the young lord of the Mamidaira Clan, Takechiyo hires Moroha as a bodyguard to help him with the familial strife at his home. During training, Kohaku teaches Towa an important lesson about learning to run away.
Zero sets a trap in the garden of Nanahoshi, a demon who feeds on sadness. Kirinmaru pays Towa, Riku, and Rion a visit. Kohaku, Hisui, and Setsuna assist the chief of the demon slayers in the north.
Kohaku and the demon slayers struggle to put out the fires caused by the Flame Bulls. Mayonaka, who used to be a local deity, demands the people of Gokoku Village hand over the town’s divine object.
Moroha learns about her parents’ battle against Shogen Mamiana, the sealing of the Full Moon Raccoon Dog, and Takechiyo’s exile from his clan. Setsuna is attacked by the snow demon Yukinyudo. Zero targets Towa on the new moon.
Moroha and Takechiyo strike back against Shogen Mamiana. Setsuna experiences her first New Moon. Towa is trapped by Nanahoshi’s eternity bugs.
Zero unearths Towa’s sadness about growing up in the modern world and corners her with her memories of loneliness and suffering. Sesshomaru appears before the demon slayers and commands Setsuna to pay the Tree of Ages a visit.
Towa is consumed by rage and loneliness. Setsuna tries to stop her from killing Zero because the curse on their mother cannot be lifted unless Zero lets go of her regrets. Sesshomaru gives Moroha the Black Pearl.
Kirinmaru takes the Black Pearl from Moroha and demands that she bring Akuru to him. Towa and Setsuna try to lend a hand, but Sesshomaru arrives at the scene to take on Kirinmaru instead. Meanwhile, Rion and Riku head to Mount Musubi.
Inside the Black Pearl, Moroha is finally reunited with her parents, Inuyasha and Kagome. Inuyasha begins to see a way out of the Black Pearl. Meanwhile, Kirinmaru’s attack leaves Sesshomaru gravely injured.
Wanting to prove his strength, Kirinmaru faces off against Sesshomaru. Towa summons the Tenseiga. Shippo waits for Inuyasha and the others at Gozu and Mezu’s gate.
In the present day, Osamu Kirin sees the Grim Comet approaching. Meanwhile, in the feudal era, Towa’s life is in danger after she uses her Zanseiken. The Spirit of the Tree of Ages orders the half-demon princesses to go destroy the Grim Comet.
To destroy the Grim Comet, Towa, Moroha, and Setsuna must travel to the present day using the Windmill of Time, but Meidomaru stands in their way. Kirinmaru takes Rion and tries to travel across time by force.
Osamu Kirin has been quietly exterminating the demons that have been appearing in the present day. He asks Towa, Setsuna, and Moroha to slay demons at the concert that is happening.
Inuyasha and the others have their hands full with the evil spirits pouring out of the burning Windmill of Time. The three girls and Osamu Kirin try to stop the Grim Comet from falling to the earth.
Osamu Kirin brings the Grim Comet to the feudal era. He convinces Rion that they are both hoping for the same world and promises to make it a reality. Meanwhile, Towa, Setsuna, and Moroha are stuck in the present day.
Towa, Setsuna, and Moroha must save Rion, who has linked her fate with the Grim Butterfly, but Osamu Kirin stands in their way. Kirin declares that he and Rion should reign over the world in order to bring about true peace.
Setsuna directs Towa and Moroha as they continue to sever Rion’s threads of fate. Each time a thread is severed, more of Rion’s true feelings are revealed. As Kirinmaru fights Sesshomaru, he realizes the real reason he lost Rion.
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.