Wing Commander is a space combat simulator intercut with live action cutscenes. Gameplay involves completing missions and destroying enemy craft, Wing commander III dispensed with the issuing of medals after such missions and relied more on cutscenes to drive the story along making much more use of CD technology. As the man giving the orders, Blair often gets to choose what ship he will fly, what missiles it will carry, and what wingman (wingmen) he will take with him. As in Wing Commander, some wingmen can be killed permanently in combat. Blair's own call sign remained customizable

The protagonist of the previous two games is officially assigned a name, Colonel Christopher Blair. Thrakhath nar Kiranka, Crown Prince of the hostile Kilrathi Empire, presides over the execution by disintegration of a group of Terran Confederation prisoners of war. One, however, is left alive: Blair's lover Colonel Jeannette "Angel" Devereaux, due to her status among the Kilrathi as a respected warrior. On the planet Vespus, Blair and Brigadier General James "Paladin" Taggart inspect the downed wreckage of the TCS Concordia. The carrier is a total loss. It is the year 2669, and the Terran-Kilrathi War has been going for over thirty years, with no signs of stopping. Blair, by orders of Admiral Geoffrey Tolwyn, is transferred as Wing Commander to the TCS Victory, a Ranger-class carrier twice as old as Blair. Her captain, William Eisen, has been with her for many years, and is proud of his ship. There are a few old faces—Colonel Ralgha nar "Hobbes" Hhallas, and Major Todd "Maniac" Marshall—but all the other pilots and staff are people Blair has never met. Among those on board, Blair meets Lieutenant Robin "Flint" Peters and Chief Fighter Technician Rachel Coriolis. Cast: Mark Hamill as Col. Christopher "Maverick" Blair Malcolm McDowell as Admiral Tolwyn John Rhys-Davies as Thrakhath nar Kiranka (voice) and James "Paladin" Taggart Jason Bernard as Capt. William Eisen Tom Wilson as Maj. Todd "Maniac" Marshall Ginger Lynn Allen as Rachel Coriolis