The events of Growlanser III: The Dual Darkness take place long before those described in the first game of the series, effectively making it the prequel. The entire planet is in danger, since the sun's energy is being gradually depleted. Two powerful countries try to seize control of the land: the kingdom of Aggressival and the Xironia Federation. The player takes control of Slayn Wilder, a young man with amnesia. Following a battle against Aggressival soldiers, Slayn is rescued by a girl named Annette, who turns out to be the daughter of the president of Xironia Federation. Together, they decide to uncover the secrets of Slayn's past, and find a way to stop the war and save the planet.

Growlanser III retains many elements of the previous games - free movement during battles, the addition of real-time element to the turn-based system, the Ring Weapon system from the previous game, etc. It also introduces new gameplay elements, such as magic combinations and skill growth. However, the most notable change in the game is the emphasis on "pure" RPG aspects and the reduction of strategy elements to the point that it cannot be qualified as a true strategy game. The party is reduced from eight controllable character to four; instead of being dictated by the story, most battles occur randomly; the player is able to physically move and explore the world map, towns, dungeons, etc.

The dating element is still present; instead of a branching storyline (as in the previous game), the dating largely depends on character creation (determining Slayn's blood group, etc.). Dialogue choices, however, are still plentiful, and different endings can be reached depending on the relationship level the player has reached.