When the Primagen's Lightship was destroyed at the end of Turok 2: Seeds of Evil, the chain reaction it triggered was so powerful that the universe as it existed was completely eradicated, pushing Oblivion, a monstrous cosmic entity that consumes bodies of the living and reigned before the birth of the universe, to the very brink of destruction. Though totally ravaged, Oblivion survived and now desperately seeks a means to punch through the Netherscape that separates the living world from the Lost Lands, a strange and primitive world where time has no meaning. The last shreds of the pure energy source that created the living world and nearly wiped out Oblivion are contained within the Light Burden, the bag that every member of the Turok lineage has carried. Deep within the Lost Lands, Oblivion's henchmen have a massive headquarters from where they assemble their armies and direct their operations.

The game begins with the current Turok, Joshua Fireseed, having dreams of a child that must be protected, as he is the last of the Fireseed lineage. During that night, Oblivion Spawns teleport into his home and try to kill Joshua in his sleep. Joshua catches them and fights, but is outnumbered. He then tells his sister Danielle and his brother Joseph to escape, while he stays behind with a bomb in his hand to blow the Spawns away, along with himself. While Danielle and Joseph drive away, they are attacked by a monster, but Adon, a female alien who helped Joshua in the previous game, saves and teleports them to a council meeting to deal with the situation of Oblivion. They decide that either Danielle or Joseph must become the next Turok, and the player must choose. The player will eventually have to infiltrate the enemies' headquarters to destroy the scourge of the universe.