Starhawk is a third-person shooter and the spiritual successor to Warhawk. The game retains the large-scale mayhem of the earlier title, combining dogfights with flying mechs called Hawks, with ground based warfare using vehicles or regular infantry fighting. Players are able to run around and shoot as in a regular action game, but can also board tanks and other vehicles, or enter Hawks that directly transform to enable flight. The two major additions compared to the earlier title are a full singleplayer campaign and real-time strategy elements with the Build n' Battle system that allows the character to construct buildings directly from the battlefield.

The singleplayer campaign is set in the distant future where humans colonize other planets in the galaxy. They mine Rift Energy, a valuable resource, but with a dangerous edge. Exposure to the energy can transform humans into savage mutants who call themselves Outcasts. They attack the mining sites, including the farm of protagonist Emmett Graves who runs it with his brother Logan. When it is destroyed, both brothers are exposed to the energy, but only Logan mutates as Emmett receives a regular implant from his friend Sydney Cutter. Emmett and Sydney become Rift Savages, mutant hunters, but eventually meet Logan again who has become the leader of the Outcasts. The story then unfolds as a large-scale battle with the two brothers in the center.

Next to the regular fighting a certain amount of time is spent building structures. By destroying opponents, vehicles and structures, and completing missions, Rift Energy is collected. There are also rift barrels in the environment that contain it. The currency is divided into orbs and cells. Ten orbs grant one cell and up to twelve cells can be held. It serves as a currency to construct buildings, which are then dropped from space. The different structures include walls, corrals, garages, auto turrets, watchtowers, outposts, supply bunkers, A.R.M.s, vulture stations, launch pads, beam turrets, depots, and shield generators. They have both offensive and defensive capabilities and are necessary to hold back the large amount of enemy units. Some structures provide vehicles and some can also be upgraded.

Multiplayer is available for up to 32 players in a single game. The Build n' Battle system is also present there with a limit of 32 structures per team. The game modes include Capture the Flag, Death Match, Team Death Match, and Zones. The latter is a Domination or Conquest type of game where players attempt to take over and hold Rift rigs, which then act as new spawn points. Multiplayer includes a persistent experience system with various skills that can be unlocked and equipped. The game can also played cooperatively, both offline and online, with up to two or four players respectively.