A group of small but vicious escaped alien prisoners called Crites descend on earth, pursued by two shape-shifting bounty hunters.
On an asteroid prison, a group of dangerous aliens known as Crites are set to be transported to another station. The Crites engineer an escape and hijack a ship, prompting the warden to hire two shape-changing bounty hunters to pursue them to Earth. Studying life on Earth via various satellite television transmissions, the first bounty hunter assumes the form of rock star Johnny Steele, while the second remains undecided, thus retaining his blank, featureless head.
Out in space on a desolate planet, the shape-shifting bounty hunters Ug and Lee and their human companion Charlie McFadden search for a vicious, worm-like creature. After killing the beast, they depart the planet. Soon afterwards, they receive a new assignment by Zanti, head of the High Council. He tells them that Critters are still on Earth and must be destroyed. With that, they set a course for Earth. Noticing Charlie brooding, Ug inquires what is wrong. Charlie states his reluctance to going back after two years and asks, concerned, whether they would leave him there. Ug assures him they have no such intentions.
Sometime after the events in ''Critters 2: The Main Course'', Charlie MacFadden is tracking down the last of the Critters. A family of three – Annie (the main protagonist), Johnny (her little brother) and Clifford (the father) – stops at a rest stop when their car's tire pops. At the rest stop, Charlie warns them and Josh, stepson of a corrupt landlord, about the Critters. As this happens, a Critter lays eggs under the family's car and the family leaves, unknowingly taking the eggs with them. Soon after they arrive at their tenement, the Critters hatch and attack the sleazy maintenance man, Frank. When the landlord arrives, he too is eaten by the Critters after Josh locks him in Clifford's room, unknowingly trapping his stepfather with the creatures. Next, one of the residents is attacked and wounded. Annie, her family and five others (including Josh) try to get to safety in one piece by getting to the roof of the building. Charlie arrives and destroys the remaining Critters, saving the remaining tenants. The film ends in a cliffhanger as Charlie is about to destroy two Critter eggs, but is ordered not to and a containment pod sent from the Intergalactic Council crashes into the basement.
The film begins where the Critters 3 left off, as Charlie McFadden (Don Keith Opper) still in his role as an alien bounty hunter, is about to destroy two Critter eggs. He is suddenly stopped by a hologram message from his alien friend Ug (Terrance Mann), who tells him the eggs are the last two Critters in existence and that it is against an intergalactic law to cause their extinction. Charlie protests that the Critters are too dangerous to keep alive, but he obeys Ug's orders to place the eggs in a preservation capsule that suddenly falls from the sky. As Charlie puts the eggs in the pod, the hatch closes on him and he is launched into space.
Follows 20-year-old Drea, who reluctantly takes a job babysitting for a professor of a college she hopes to attend. Struggling to entertain the professor's children Trissy and Jake, along with her own little brother Phillip , Drea takes them on a hike, unaware that mysterious alien critters have crash-landed and started devouring every living thing they encounter.
The Critters return to Earth searching for a lost friend that was left behind. They land in Burbank and soon torment a group of high-schoolers and their families.
