Jeffrey Hunter played the commanding officer of the USS Enterprise, Captain Christopher Pike, in the rejected Star Trek television pilot "The Cage". In developing a new pilot episode, called "Where No Man Has Gone Before", series creator Gene Roddenberry changed the captain's name to "James Kirk" after rejecting other options like Hannibal, Timber, Flagg and Raintree. The name was inspired by Captain James Cook, whose journal entry "ambition leads me ... farther than any other man has been before me" inspired the episode title. The character is in part based on C. S. Forester's Horatio Hornblower hero, and NBC wanted the show to emphasize the captain's "rugged individualism". Jack Lord was Desilu Productions' original choice to play Kirk, but his demand for fifty-percent ownership of the show led to him not being hired. The second pilot episode was successful, and "Where No Man Has Gone Before" was broadcast as the third episode of Star Trek on September 22, 1966.

Shatner did not expect Star Trek to be successful, so when it was cancelled in 1969, he assumed it would be the end of his association with the franchise. He went on to voice Kirk in the animated Star Trek series, star in the first seven Star Trek films, and provide voice acting for several games. Star Trek II: The Wrath of Khan Director and Writer Nicholas Meyer, who had never seen an episode of Star Trek before he was assigned to direct, conceived a "Hornblower in outer space" atmosphere, unaware that those books had been an influence on the show. Meyer also emphasized parallels to Sherlock Holmes, in that both characters waste away in the absence of stimuli: new cases for Holmes; starship adventures for Kirk.

According to Shatner, early Star Trek reviewers described his performance as "wooden", with most of the show's acting praise and media interest going to Nimoy. However, Shatner's mannerisms when portraying Kirk have become "instantly recognizable" and Shatner won a Saturn Award for Best Actor in 1982 for The Wrath of Khan. Star Trek II Director Nicholas Meyer said Shatner "gives the best performance of his life" in The Wrath of Khan. The Guardian called Pine's performance of Kirk an "unqualified success", and The Boston Globe said Pine is "a fine, brash boy Kirk". Slate, which called Pine "a jewel", described his performance as "channel[ing]" Shatner without being an impersonation.

In 1985, Riverside, Iowa petitioned Roddenberry and Paramount Pictures for permission to "adopt" Kirk as their town's "Future Son". Paramount wanted $40,000 for a license to reproduce a bust of Kirk, but the city instead set a plaque and built a replica of the Enterprise (named the "USS Riverside"), and the Riverside Area Community Club holds an annual "Trek Fest" in anticipation of Kirk's birthday.

Kirk has been the subject of a wide range of television spoofs that aired in many countries, including The Carol Burnett Show and KI.KA's Bernd das Brot. John Belushi's impression of Kirk for Saturday Night Live, which he described as his favorite role, was "dead-on". Jim Carrey has been praised for his satire of the character in a 1992 episode of In Living Color. Comedian Kevin Pollak is well known for his impressions of Shatner as Kirk. Kirk has also been mentioned in song, the 1984 English adaptation of "99 Luftballons" as well as in the German original by Nena and the 1979 song "Where's Captain Kirk?" by Spizzenergi.

Kirk has been merchandised in a variety of ways, including collectible busts, action figures, mugs, t-shirts, and Christmas tree ornaments. A Kirk Halloween mask was altered and used as the mask worn by the character Michael Myers in the Halloween film franchise. In 2002, Kirk's captain's chair from the original Star Trek was auctioned for $304,000.

James Cawley has played Kirk in the Phase II series since it began in 2004. Wired observes that while Cawley's depiction "lacks Shatner's vulnerability", the actor has enough swagger "to be passable in the role". Cawley's portrayal was well-known enough at Paramount that a group of Star Trek: Enterprise Writers called for Cawley's attention at a science fiction convention by shouting "Hey, Kirk!" at him while Shatner sat nearby.

In Star Trek (2009), screenwriters Alex Kurtzman and Roberto Orci focused their story on Kirk and Spock in the movie's alternative timeline while attempting to preserve key character traits from the previous depictions. Kurtzman said casting someone whose portrayal of Kirk would show that the character "is being honored and protected" was "tricky", but that the "spirit of Kirk is very much alive and well" in Pine's depiction. Due to his belief that he could not take himself seriously as a leader, Pine recalled having difficulty with his audition, which required him "to bark 'Trek jargon'", but his charisma impressed Director J. J. Abrams. Pine's chemistry with Zachary Quinto, playing Spock, led Abrams to offer Pine the role. Jimmy Bennett played Kirk in scenes depicting the character's childhood. The Writers turned to material from the novel Best Destiny for inspiration as to Kirk's childhood.

In a 2010 Space Foundation survey, Kirk tied with cosmonaut Yuri Gagarin as the No. 6 most popular space hero.

In preparing to play Kirk, Pine decided to embrace the character's key traits – "charming, funny, leader of men" – rather than try to fit the "predigested image" of Shatner's portrayal. Pine specifically did not try to mirror Shatner's cadence, believing that doing so would become "an impersonation". Pine said he wanted his portrayal of Kirk to most resemble Harrison Ford's Indiana Jones or Han Solo characters, highlighting their humor and "accidental hero" traits.

In scientific Illustrator Jenny Parks' 2017 book Star Trek Cats, Kirk is depicted as an orange tabby cat.