In earlier times, the world was ravaged by endless war and conflict. The fighting only ceased when five sisters with godlike powers used their song magic to defeat the warlords and bring peace throughout the lands. These Intoners now rule over various parts of the world, where they are adored and worshipped by their subjects. However, there is a sixth and eldest sister, Zero, who wishes to kill her siblings and take their power for herself. One year after failing to defeat the other Intoners, Zero sets out with her dragon Mikhail to kill them one by one.

Taking place about a century prior to the first Drakengard, this game puts the player in the role of Zero, who can be accompanied by up to two AI characters who join over the course of the story. Gameplay is largely similar to other entries in the series, comprised of hack-and-slash fighting on the ground and aerial combat in which Zero rides Mikhail. Performing combos fills up Zero's Tension Gauge, which she can tap into to unleash her Intoner powers. In Intoner Mode, Zero's speed and attack power increase, and she becomes invulnerable to enemy attacks. Zero can use four different types of weapons: swords, bracers, chakrams, and spears, and each individual weapon can be leveled up the more it is used in combat.