John Robert Crichton, Jr. is an International Aeronautics and Space Administration (most commonly referred to as IASA) astronaut who is accidentally catapulted through a wormhole across the universe. Although Crichton is a heroic and unwaveringly loyal character, he is also a mischievously comical one. During a test flight designed to prove a scientific theory concerning the use of planetary gravity as a means for spaceship acceleration, a wormhole appears, and John and his 'Farscape One' module are pulled into and through it. On his exit from the wormhole, he finds himself in the middle of a spaceship dogfight, during which he accidentally causes the death of Tauvo Crais, the brother of Peacekeeper Captain Bialar Crais. Crichton's craft is pulled aboard a large spaceship named Moya, a Leviathan, where John meets his first aliens (Zhaan, D'Argo, Aeryn Sun and Rygel). Shortly after, John meets Bialar Crais, who wants revenge for his brother's death. John has to adapt rather quickly to a life with aliens, guns, and space travel, without the comfort of Earth culture. Crichton encounters a mysterious alien race known only as The Ancients, who hide a repository of wormhole knowledge into his brain to guide him home, beginning a long chase by a Sebacean-Scarran hybrid Peacekeeper called Scorpius who hunts John and the rest of the crew to obtain that information.
Crichton learns that Scorpius has implanted a neural chip into his head, which causes hallucinations of a 'neural clone' of Scorpius, whom he dubs "Harvey". These hallucinations influence Crichton in an effort to get at the hidden wormhole knowledge. As a result, Crichton's behavior grows more erratic and unpredictable, even as he continues to have romantic feelings for Aeryn Sun. The neural chip takes complete control over Crichton (resulting in a Scorpius/Crichton mixed personality with extremely dark humor) and transmits a message to Scorpius. Shortly after that Harvey defeats Aeryn in an aerial dogfight and seemingly kills her. After Aeryn's death, Crichton regains control. The chip is removed, but stolen by Scorpius. Harvey still remains in Crichton's head, and Aeryn has been revived by Zhaan, who consequently dies later. Some time thereafter Crichton is "twinned" by another alien; neither of the Crichtons can be called a copy, but are "equal and original" (and each has his own "Harvey"). Eventually, the crew of Moya is split across the two Leviathans, Moya and Talyn, and they are subsequently separated from each other; each ship has one Crichton. The Crichton aboard Talyn begins a romantic relationship with Aeryn while the Crichton on Moya continues studying wormholes, helped by the repository in his brain. Jack the Ancient finds the Talyn Crichton, forcibly extracts Harvey and unlocks the wormhole knowledge, but this Crichton later dies of radiation poisoning from a wormhole weapon. When the survivors of the two crews are reunited, Aeryn (in her grief) is very cold to the remaining Crichton, due to him having different memories about the last few months; the crew members of Moya start going their separate ways. Just after Aeryn Sun leaves Crichton, seemingly for good, he learns that she is pregnant with his child.
This leaves Crichton with nothing but time to work on his wormhole theories. He eventually reunites with the crew members of Moya and Aeryn and Scorpius, who has fallen out of favor with Peacekeeper high command. Shortly, after arrival, Scorpius offers to remove Harvey. Due to the neural clone's longer presence within and increased familiarity with Crichton, Harvey's reaction includes persuasion and appeal to sympathy rather than threats. Crichton still agrees to allow Scorpius to remove the lingering neural spillover. Crichton finds his way back to Earth, but he voluntarily gives up the dream of Earth and returns to Moya. After a series of dangerous events (including Harvey's resurrection), Crichton and Aeryn find time alone together. Aeryn tells him he is the father of her child, and Crichton proposes to her. The moment she accepts, an alien craft melts the two.
Crichton and Aeryn are revived at the beginning of The Peacekeeper Wars, and Crichton uses his wormhole knowledge to successfully force a peace treaty between the warring Peacekeepers and Scarrans. The wormhole knowledge in his brain is finally removed by Einstein the Ancient. Aeryn gives birth to their son named D'Argo Sun-Crichton in honor of their late comrade.