In the fourth planet of the Lylat System,Corneria,The evil Andross turned this once thriving system into a wasteland of near extinction. General Pepper successfully exiled him to a deserted planet,Venom. Five years later,General Pepper noticed strange activity coming from Venom. The Star Fox Team led by James McCloud were sent to investigate. Upon their arrival,The Team's member,Pigma Dengar betrayed them and has James and his friend Peppy Hare captured by Andross. James manage to sacrifice himself to allow Peppy to escape and tells James' son,Fox what has happened.

A few years later,Fox goes to the Academy where he met Falco Lombardi and Slippy Toad. Andross' Army invaded Corneria. Fox manage to stop them with Falco and Slippy's help. After this,The Star Fox Team is reborn.

They are joined by Peppy,Bill,Fay,Katt,and Miyu. Andross learns about this and has his Nephew,Andrew Oikonny join the members of the Star Wolf Team,Wolf O'Donnell and Leon Powalski,along with Pigma.

At Corneria,General Pepper sends the Star Fox Team to recover their stolen army base from the Venomian Invader Fighters. By the time they got here,The Star Wolf Team attacks the Star Fox Team. After Andrew's Wolfen's Wing gets damaged,Grangar aids the Star Wolf in his Mech. ROB 64,the Team's robotic operator,detected the bomb that the Star Wolf planted is inside the base. Fox managed to stop it while Falco and Slippy took down the Mech,killing Grangar.

The Star Fox Team must go to Venom to stop Andross. While there,They are confronted by Star Wolf again. After Pigma gets shot down,Wolf and Leon retreats,but not before Peppy's Arwing gets damaged. Fox confronts Andross and fires several shots. After his outer layering of his head gets destroyed,Andross reveals his true form: an enormous brain with bulging eyes. Fox manage to blasts Andross,causing him to burst into flames.

Fox quickly escape with the help of James' Spirit as Andross exploded. Back at the Great Fox,General Pepper declared the Star Fox Team as heroes.

Mid-Credits:
Pigma survived the crash,calling out,but no reply.