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It is the middle of the 22nd century. Mankind has reached a point in it’s technological advances to enable colonization of the far reaches of the universe. Armed with Exponential Thermosteller Bombs, the scout ship DARK STAR travels out on the very rim of the known universe, far in advance of colony ships, prowling the unstable planets. Meanwhile the crew of Doolittle, Pinback, Boiler and Talby perform their jobs in a state of abject boredom.

The plot follows the misadventures of the four man crew of the Dark Star. The ship has been in space for twenty years on a mission to destroy "unstable planets" which might threaten future colonization. Comedic disaster is the order of the day, as the tedium of their task has driven the crew up the wall. Their Commander, Powell, has died and exists only via cryogenic supports. Sgt. Pinback has adopted a ship’s mascot in the form of a mischievous alien "beachball with claws" that refuses to stay put. Lt. Doolittle dreams of surfing back in Malibu. Ship’s Navigator Talby has become reclusive in the ships done. The computer has become dysfunctional due to damage suffered in an asteroid storm, and subsequently Bomb #20 is threatening to detonate while still in the ship’s bay. Lt. Doolittle revives Commander Powell who advises them to teach "Phenomenology" to the Bomb. The Bomb interprets that it is God… and with the line, "Let there be light!"…explodes, sending the ship and crew into infinity as Talby drifts off into the Phoenix Asteroids and Doolittle surfs off into the Veil Nebula.

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