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.

與麒麟丸一戰，讓剎那失去了性命。在深深懊悔的永遠面前出現的殺生丸說“要讓剎那生或者死，都取決於你”，將折斷了的天生牙交給了她。永遠想像菊十文字那樣製作出妖氣刀身，然而天生牙卻沒有變化。反而是失去妖氣的永遠，像朔那樣頭髮逐漸變黑。讓剎那復活已經不可能了嗎？刀刀齋用瑠璃玻璃和灰土製作出了與剎那的血刀相稱的薙刀相贈。

為了尋找刀刀齋所提到的，能對抗麒麟丸的武器·吸妖魂之根而來到海邊村莊的永遠，得知了會襲擊擁有美麗長發的女性的“海蛇女”的傳聞。她似乎原本是守護這一帶海域的妖靈“海神的玉姫”。另一邊，諸葉和剎那救下的海邊尼姑庵的女尼，正是那海蛇女。面對只要目視對方眼睛就會被變成石頭的海蛇女，沒有有效的攻擊手段，二人陷入困境，這時永遠和退治屋趕到。

十四年前是露給鈴施下銀鱗詛咒。施加了詛咒的銀鱗覆蓋全身之時，鈴就會死亡。為了延緩進度，向時代樹精靈詢問方法的邪見，在由於森林火災和永遠分開的年幼剎那脖子上掛上了夢之蝴蝶的蛹。另一邊，尋找樸仙翁的永遠等人，遭遇要消滅殺生丸之女的妖怪們的追擊。讓另外二人先離開，剎那獨自一人面對敵人，這時理玖出現，擊退了妖怪。剎那詢問理玖的真實意圖。

永遠她們踏進吸妖魂的根所在的產靈山，被邪惡的妖力設下的結界困住。只有擁有靈力的諸葉通過結界，遇見麒麟丸的女兒璃音…。

璃音請求剎那斬斷找到自己的父親與自己之間的孽緣。並交給永遠一個麒麟丸唯一害怕的武器，吸妖魂的根做成的「星碎之笛」，卻遭到妖靈獸攻擊。

剎那在睡覺時不知不覺被拐走。醒來後在扇谷柊家裡，受到愛史姬委託，假扮成不情願的替身公主。但是，前來教導她的尼姑竟然是化身成姊姊金烏的翡翠。

為了解決家鄉的騷動，前往故鄉狸穴島的竹千代僱用諸葉當自己的助手。另一邊，琥珀帶著剎那一起去收拾雪乃國的妖怪，戰鬥方式太危險的永遠被留下來。

用香木「小銀河」把人們的悲傷轉化成香氣享受的妖怪七星。盯上永遠性命的是露在七星的庭院裡設下陷阱。琥珀他們受雪乃國五穀村僱用，出發去收拾炎牛。

琥珀他們為了撲滅炎牛噴出的烈火四處奔走。五穀村的村民們告訴剎那，被迫在魔夜中獻出神佛「五穀的恩惠」，是因為土地神自己變成了鬼神的關係。

八衛門狸說出了滿月狸被封印的過去和竹千代的英勇事蹟。此時，雪入道攻擊旅館，使得剎那陷入危機。在七星的庭院設下陷阱的是露，盯上在新月的夜晚失去力量的永遠。

與大家老．將監的對決完滿結束，諸葉開始和竹千代一起反擊。另一方面，新月之日，剎那寫下對付雪妖怪的辦法後睡著了。永遠也失去妖力，被常世蟲附身陷入困境。

憎恨夜叉姬的是露，打算讓在現代社會長大的永遠飽受孤獨和悲傷記憶帶來的痛苦。另一方面，出現在琥珀等人面前的殺生丸，命令剎那前往時代樹。

從諸葉手中取走黑色珍珠的麒麟丸命令她將阿久留帶過來，殺生丸也出現在來到那裡永遠和剎那面前…。另一邊，璃音和理玖一起前往產靈山。

與永遠和剎那一起被送進黑色珍珠裡的諸葉，終於與父母犬夜叉和阿籬重逢。犬夜叉注意到逃出黑色珍珠的關鍵在於永遠和天生牙。另一邊，滿身是傷的殺生丸將會…。

殺生丸與麒麟丸對峙。殺生丸手邊的天生牙在永遠的召喚之下，出現在永遠那裡。永遠將全身的妖氣注入天生牙。而另一邊，七寶在牛頭馬面的門前守候犬夜叉他們…。

在現代的希林獨自察覺到妖靈星接近。在戰國時代，用了斬星劍的永遠耗盡靈魂。而另一邊，時代樹精靈命令夜叉姬去摧毀即將在令和時代墜落的妖靈星。

為了摧毀令和的妖靈星，打算穿越時空的永遠她們，前往能看到時之風車的殺生丸和母親的住所。可是，為了妨礙時之風車轉動的冥道丸擋住了她們的去路。

回到現代的永遠她們找到希林理之後，接下他的委託，到朱利安所屬的偶像團體6x's的現場演唱會會場幫忙除妖。那隻妖怪的出現也與妖靈星相關。

著火的時之風車大門湧出大量的魑魅魍魎。犬夜叉他們為了阻止災害挺身而戰。在另一邊的現代，希林理自告奮勇，協助永遠她們阻止妖靈星墜落地面…。

回到戰國時代的希林理，打算與璃音利用吸妖魂的力量，一起改變世界。阿久留實現了留在現代的永遠她們的心願，打開時空之門。離別之際，草太告訴永遠…。

為了救出被困在妖靈蝶裡的璃音，潛入其中的永遠等人被希林理擋下，麒麟丸賭上最強的名號，向殺生丸提出挑戰，犬夜叉等人則是試圖封印妖靈蝶的行動…。

在砍斷緣之線的同時，永遠、剎那和諸葉聽見了璃音的心聲。她和麒麟丸能化解後悔和誤會，重拾父女的羈絆嗎？另外，殺生丸和麒麟丸的決戰結果是…。

為了替諸葉還清欠債，犬夜叉鼎力相助。諸葉向永遠和剎那介紹一份有趣的工作，邀請她們前來屍屋，三人在那裡結識一位奇妙的男子，委託她們去伊予之國除妖。