In the mid-22nd century, mankind has begun to colonize interstellar space. Armed with artificially intelligent Thermostellar Triggering Devices, which can talk and reason, the scout ship Dark Star searches for "unstable planets" which might threaten future colonization.
Twenty years into its mission, the Dark Star has aged and suffers frequent malfunctions. Commanding officer Powell has died in one such event, but remains aboard in cryogenic suspension. Lieutenant Doolittle, a former surfer from Malibu, has taken over as commander. The tedium of their work has driven the crew of Pinback, Boiler, and Talby "around the bend", so they have created distractions for themselves.
Pinback plays practical jokes, maintains a video diary, and has adopted a ship's mascot in the form of a mischievous "beach ball"-like alien who refuses to stay in a storage room. After it attempts to push him down an elevator shaft, he eventually kills it with a gun. He claims to really be Bill Froug and says that the real Pinback has committed suicide.
En route to their next target in the Veil Nebula, the Dark Star is hit by electromagnetic energy during a space storm, resulting in another on-board malfunction. Thermostellar Bomb #20 receives an erroneous order to deploy, but the ship's computer talks it back into the bomb bay. An accident with a laser then causes more mayhem, damaging the ship's computer. Bomb #20 deploys again, and this time the crew cannot convince it to stand down. Doolittle revives Powell, who advises him to teach the bomb phenomenology. Doolittle space walks out to have a philosophical conversation with the bomb. It agrees to disarm itself for the moment.
Pinback opens the airlock to admit Doolittle, but accidentally ejects Talby, who was in the airlock attempting to repair the laser. Doolittle leaves the ship to retrieve Talby, who is in a space suit but has no maneuvering device. The bomb, having learned Cartesian doubt, trusts only itself. Convinced that only it exists, and that its sole purpose in life is to explode, it does so. Dark Star is destroyed, along with Pinback and Boiler. Talby and Doolittle, at a distance from the ship, are thrown clear. The former drifts into the Phoenix Asteroids, a cluster with which he has long been fascinated. Doolittle, falling toward the unstable planet, finds an oblong hunk of debris, and surfs into the atmosphere, to die as a falling star.
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