In a Japan where ancient monsters known as Makamou prey on humanity, a secret organization called Takeshi has for centuries trained warriors called Oni to fight these beasts using the power of pure sound. Unlike traditional Kamen Riders who use punches and kicks, the Oni wield specialized instruments as weapons, defeating their enemies through attacks called Ongeki, or sound strikes. The series follows Hitoshi Hidaka, a seasoned and easygoing Oni known as Kamen Rider Hibiki, who uses drumsticks as his weapons of choice.

The story is largely told through the eyes of Asumu Adachi, a timid fourteen-year-old boy on the verge of high school who feels lost about his future. After witnessing Hibiki battle a Makamou, Asumu becomes fascinated with the warrior and begins following him, leading to an unofficial teacher and apprentice relationship. Unlike previous series where the protagonist is a young man learning to fight, Hibiki is already an experienced hero, and the narrative focuses instead on Asumu's coming-of-age journey as he learns life lessons from Hibiki and the other Oni.

The Oni operate under the support of Takeshi, which provides them with intelligence, equipment such as small robotic helpers called Disk Animals, and a network of branches across Japan. Key supporting characters include Ichiro Tachibana, the cheerful head of the Kanto branch; his daughters Kasumi and Hinaka, who handle field support and monitoring; and Midori Takizawa, the eccentric inventor of the Oni weapons. Among the other Oni are Iori Izumi, known as Kamen Rider Ibuki, a composed young man who uses a trumpet-like weapon; and Tomizo Todayama, the enthusiastic Kamen Rider Todoroki, who plays a guitar-like instrument and trains under his stern master Zanki.

For the first twenty-nine episodes, the series maintains a gentle, atmospheric tone with a focus on character development, nature, and traditional Japanese aesthetics. Episodes often follow a pattern where a Makamou appears, the Oni track it, and Hibiki or another Rider defeats it using a specific sound-based finisher. The Makamou are often accompanied by two mysterious childlike figures known as Douji and Hime, who serve as harbingers of a coming catastrophe.

A significant shift occurs beginning with episode thirty, when the production staff changes, including new head writer Toshiki Inoue. The series adopts a more conventional superhero drama tone, with increased interpersonal conflict and a faster pace. A year-long time skip introduces new characters, including Kyosuke Kiriya, a brash teenager who declares himself Hibiki's rival and eventually gains the ability to transform into an Oni himself. The later episodes build toward the awakening of a massive, god-like Makamou called Orochi, forcing all the Oni to unite for a final battle.

The series concludes with the Oni successfully defeating Orochi, though the victory comes with sacrifices, including Zanki's near-fatal injury. Asumu, having grown more confident through his experiences, decides not to become an Oni but instead pursues his own path toward becoming a doctor. The final episode ends on an open note, showing Hibiki continuing his training and Asumu moving forward with his life, emphasizing that the fight against the Makamou will continue indefinitely.