It is several years after the end of mankind's war against the Kilrathi. Col. Christopher Blair is called back into active duty by the Terran Confederation to help stop acts of terrorism that appear to be taking place against Confed by Border Worlds forces. But it soon becomes clear that the enemy may not be them at all when Blair and several of his friends defect to Border Worlds forces to try to find out who the real culprits are and to prevent the Confederation and the Border Worlds from entering into the chaos of an intergalactic war....

Whereas the video inserts for Wing Commander III had been shot on video in front of a green screen to color key the actors into computer generated sets, Wing IV was shot on film using real sets on a sound stage at Ren-Mar Studios in Hollywood.

Admiral Tolwyn:
Mankind was at its zenith when fighting the Kilrathi. Now we stroll about complacent and confused. Who is going to save us when the next race tries to dominate us? Who knows where that attack will come from and when? No, we must be prepared.