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The game begins soon after the Battle of Hoth. The player assumes the role of a rookie TIE fighter pilot. Despite playing on the side of the Star Wars saga's "villain", the player's role is somewhat sympathetic, not only because he lives in fear under the shadow of Darth Vader and other unforgiving superiors, but also because the game's portrayal of the Empire—dictated, of course, by the player's superiors—focuses on its role as a guardian of order. The main character of TIE Fighter is Maarek Stele, although his name is only revealed in the official strategy guide as well as a novella entitled The Stele Chronicles that came with the initial release versions of the game.

Instead of constantly fighting against the Rebels, many missions deal with the elimination of pirates and other criminals, as well as civil wars, traitorous Imperials, and otherwise maintaining order in the galaxy.

In addition to the standard mission briefing, there is a secondary briefing available in some missions, given by a mysterious figure who belongs to the Emperor's Inner Circle. This person briefs the pilot on the secondary and optional objectives. Successfully completing them doesn't alter the scenario or the overall success of the mission, but initiates the pilot in an Imperial "secret society." These secondary briefings also reveal significant plot points, such as evidence of Admiral Harkov's treason.