現代でごく普通に暮らす中学3年生の女の子・日暮かごめは、 ある日突然戦国時代にタイムスリップ。 50年前に巫女・桔梗に封印された半妖の少年・犬夜叉と出会う。 かごめは自分の体の中から出てきた「四魂の玉」を悪しき者たちが狙っていることを知る。 妖怪の力を強める働きがあると言われている四魂の玉。桔梗の生まれ変わりであるかごめには、その玉にまつわる不思議な力があるらしい。 しかし、四魂の玉は妖怪との戦いで砕け散ってしまった。ここに、かごめの力で封印を解かれ、50年の眠りから目覚めた犬夜叉と、時を越えた旅人かごめの、四魂の玉のかけらをめぐる大冒険が始まった！ 50年前に犬夜叉と桔梗を罠にはめ、弥勒一族に風穴の呪いをかけた因縁の男・奈落や、犬夜叉の刀・鉄砕牙を狙う兄・殺生丸など、数々の敵たちとの激闘。コギツネ妖怪・七宝、不良法師・弥勒、妖怪退治屋・珊瑚といった仲間達との出会い。そして、蘇った桔梗と、かごめ、犬夜叉の三角関係の行方は!? 舞台は戦国。それぞれの想いを胸に、彼らの旅は果てしない広がりをもって続く…。
Inuyasha's father defeated a powerful Chinese yōkai moth named Hyōga, five hundred years ago. The Shikon Jewel shard revives his son, Menōmaru, and his loyal servants, Ruri and Hari (who plan to avenge their family). When Miroku and Sango meet the duo, Ruri copies the wind tunnel and Hari possesses Kirara. Menōmaru kidnaps and places a spell on Kagome. He breaks the seal to release the power of his predecessor. Though becoming stronger, he achieves the title of the clan. While staying at the fortress, Menōmaru uses the spell to possess Kagome. Inuyasha attempts to evade Kagome, when he discovers that she is wearing Kikyō's clothes. Kagome inadvertently kills Inuyasha, pinning him with an arrow on "The Sacred Tree" (like Kikyō did to him fifty years ago). After Kagome resists the spell, she apologizes to Inuyasha. When Kikyō tells Kagome that she does not belong in the feudal era, she sends her to the "Bone-Eater's Well". A grief-stricken Kagome ends up returning in the present day and wanders though Tokyo. After sensing that Inuyasha is alive, Kagome shoots the arrow into the well, causing it to explode. She travels back in time and reconciles with him. As Kirara resists the spell, Miroku and Sango defeat the duo. When Menōmaru emerges from the moth cocoon and reveals his giant body, Inuyasha defeats Menōmaru with Kagome's help. With everything returned to normal, Inuyasha and Kagome spend time in Tokyo.
After the heroes seemingly defeat Naraku, Inuyasha, Kagome and Shippo are separated from Miroku and Sango. Kagura and Kanna meet Kaguya, the Princess of the Heavens, being sealed in a mirror. In exchange for freeing them, Kaguya promises them to grant their eternal freedom. When they take one of the five items, Kaguya is released from the mirror and she captures Kagome. The united group head and infiltrate the castle through the realm of mirrors. There, Kaguya attempts to transform Inuyasha into a full-fledged demon, but Kagome breaks the spell and saves Inuyasha. Naraku reappears on Kohaku's back, revealing that he faked his death. The villains escape from the realm. Kagome destroys the mirror and Inuyasha does to Kaguya's body. When Kaguya appears in a gas form, she is sucked into Miroku's wind tunnel. Inuyasha and his friends escape from the realm and return to their world through the mirror. With everything reverted to normal, they resume their journey.
Two hundred years ago, Inuyasha's dog-demon father saves his human mother, Lady Izayoi from Takemaru, a samurai who had yearned for her. Izayoi and her newborn half-demon son, Inuyasha, escape from the palace, where Inuyasha's father and Takemaru died.
In Horai Island, six half-demon children (Asagi, Dai, Roku, Moegi, Shion and Ai), watch a woman (resembling Kikyō) dropping a green orb to the Cauldron of Resonance. It frees the Four War Gods (Ryūra, Jūra, Kyōra and Gōra), and the scars appear on the rest of all children. Ai, not affected by the gods, leaves the island to meet up with Inuyasha and his friends. The heroes learn that Gōra used Kikyo's blood to create her doppelganger and Ryūra placed the scar on Inuyasha, though Inuyasha and the children cannot resist it. One man tells the story about the myth of the island, before Kikyō sets out to the island. As the rest of the villagers safely head to the shrine, Sesshomaru remembers the day he got the scar. Upon arriving at the island, Inuyasha and his friends are ambushed by Jūra. While Miroku and Sango manage to distract Jūra, Inuyasha saves Kagome and Ai from Ryūra.
幼い頃、森の火事に巻き込まれ、離ればなれになった双子の少女、とわとせつな。とわは、時代樹じだいじゅの時空を越えるトンネルをくぐり抜け、戦国時代から現代へとタイムスリップ。かごめゆかりの日暮ひぐらし家の娘として育てられ、武道に長けた女子中学生に成長した。一方、戦国時代に残された妹のせつなは、妖怪退治屋のお頭となった琥珀こはくの下で妖怪退治を生業にしていた。もろはは、かごめと犬夜叉いぬやしゃの娘。賞金稼ぎとして「化ばけ殺ごろしのもろは」の異名を取り、やはり妖怪退治に明け暮れている。 とわとせつなが別れ別れになってから、10年。時代樹の時空を越えるトンネルが再び開かれた。現代に現れたせつなと再会するとわだったが、せつなは何故かとわのことを忘れてしまっていた。 せつなと共に､現代にやって来たもろはも加わり、とわたち「半妖はんようの夜叉姫やしゃひめ」が、現代を、そして戦国時代を、縦横無尽に暴れ回る！