Andross has declared war on Corneria. Lylat is in chaos. James McCloud, Corneria's best chance at an early end to the war, has been betrayed and killed by one of his closest friends. Peppy Hare, the one remaining member of James' legendary mercenary team, Star Fox, has returned home to being news of James' apparent death to his son, Fox McCloud, an aspiring pilot studying at the Corneria Flight Academy. Fox leaves behind his education and home to reform his father's mercenary team with the help of Slippy Toad, a gifted mechanic, Falco Lombardi, a reckless and immensely skilled pilot, and Peppy Hare, a veteran navigator. They quickly build a name for themselves as skilled mercenaries, and are hired by General Pepper of the Cornerian Army to stop Andross and push his invasion back. However, things are not always as black and white as they seem, and Fox soon discovers that many people he considered allies may have other motivations, or moral grey spots that they hide from the world.
James McCloud never expected to wake up after crashing through Venom's toxic atmosphere. Looking up from the wreckage of his experimental Arwing combat plane, the very air burning his lungs, he awaited his own delayed death, alone, and afraid.