Total Annihilation: Kingdoms is the fantasy spin-off title to the 1997 real-time strategy game Total Annihilation. There are four distinct factions: Aramon, Taros, Veruna, and Zhon, and each is spearheaded by their monarch unit (respectively Elsin, Lokken, Kirenna, and Thirsha) which replaces the commanders from the original Total Annihilation. In the game's storyline, these monarchs are siblings who are at each other's throats fighting for supremacy over the land of Darien after the disappearance of their father Garacaius.

Monarchs are the main construction unit in the game, but they are mostly not capable of building objects from the entire tech tree. Aramon, Taros, and Veruna rely on other construction units to do so, and the tech tree is effectively split to 3 tiers, one with each factory-type structure assigned to it. Conversely, Zhon has few structures available to them, as they rely more on units. There is only one resource, mana, which is gathered from sacred stones by structures known as lodestones. Building units and structures, as well as monarchs' special attacks, drain mana, and its input/output values are shown in the bottom right corner of the screen. Finally, monarchs have special abilities: Elsin can raise the dead and build ark ships, Lokken can become invisible and build all three Taros factory structures, Kirenna can swim (by doing so, she replaces her legs with fins), and Thirsha can fly and build a tier 2 Zhon defensive structure; they also have three attack types.

As units and structures are being summoned, they are formed as silhouettes which gradually materialize. While this is going on, they are immobile and vulnerable to attacks. Also, if the structure or construction unit responsible for the summoning is moved to a different task or destroyed, the silhouette will gradually lose health until it vanishes, but in the case of structures and Zhon units, summoning can be resumed in that small time window.

The game features 48 missions in its singleplayer campaign, which are played in succession and give player control over different factions in different points of the storyline. As was the case with the original Total Annihilation, the developers released new freely downloadable units on the official website after release.