It has been some twelve years since the destruction of Kilrah, the Kilrathi homeworld. The Terran Confederation, slowly demobilizing and reorganizing its military assets, has settled on a new strategy: building several Midway-class megacarriers, brainchild of Navy Commodore Christopher Blair. These new carriers, over a kilometer long, carry all the hardware and weaponry of a Kilrathi-War-era carrier battle group. The first one, the Midway herself, is undergoing her shakedown cruise, with Blair along for the ride. Before this, though, the player is treated to a CGI video of a bizarre rupture in space in the Kilrah system: the first of the Nephilim invaders. The game's titular prophecy involves the coming of these alien invaders, who shall arrive only after "one who has the heart of a Kilrathi, but who is not Kilrathi-born," conquers the felinoid warrior race.
The player takes the role of 2nd Lieutenant Lance Casey, son of the venerable Major Michael "Iceman" Casey from Wing Commander I.