Drakengard 3 transports players to a medieval world where six goddess-like sisters known as "Intoners" have brought peace to the earth with their power to manipulate magic through song. Harmony is disrupted, however, when the eldest sister, Zero, attempts to murder her younger sisters with the help of her dragon companion, Mikhail. As the story progresses, players find themselves in a battle to unravel the mystery of Zero and learn her true intentions. A prequel to the original Drakengard, Drakengard 3 features the series’ signature brand of action, pitting players against hordes of fiends and foes in remorseless hack-and-slash ground combat, and then sending them soaring for pitched aerial battles on the back of the dragon Mikhail.

The story focuses on Zero, a woman who can manipulate magic through song. Partnering with a dragon named Mikhail, Zero set out to kill her five sisters, who rule the world's regions. As she travels, the player discovers the true reason behind Zero's rampage.