Gameplay is divided into two main game modes: the game as a whole is called Star Citizen, whilst Squadron 42 is the name for the single player focused side of the game.
- The military path is more akin to the Wing Commander campaign. The player opts to join the navy and is recruited by Squadron 42. The player will be faced by a mission structure much more similar to a single player game, with briefings and an engaging story. When you've served your time, the game opens up, allowing you either to stay on with the military or move on to a bigger mode, with open-endedness and galaxy persistence. Although the military path can be played and enjoyed in single player mode, friends can also join your game for online cooperative gameplay via a drop-in feature. Because this feature worked well in the video game Dark Souls, a similar feature has found its way into this game.
- The open path starts you out without any ties to the military, and promises a more varied mercenary-like experience where you are your own boss, choosing how you earn your place. In this mode the game is described to be an online multiplayer Freelancer/Privateer experience.

These two modes mean that you can skip the structured military campaign and join the more open game straight away if you want, although both stats and credits you earn from your single player game will transfer over to the open online game.
The game aims to simulate the entirety of its universe to allow the players some extra level of immersion. Player statistics will be tracked and saved throughout gameplay, such as how much money you have, your civic status, the ship you fly, it will all be there next time you load up the game.
A virtual economy system will also play an important part of this game's universe.


