In 2271, to combat the V'Ger Crisis, Admiral Kirk accepted (though "took" may be more accurate) temporary command of the Enterprise over Captain/Commander Willard Decker who oversaw its refit while in dry dock. After the subsequent disappearance of Decker, Kirk appeared to take command of the vessel. It has long been suggested that a second five-year mission of the Enterprise followed, however this has never been established in the canon. Nor has speculation that Kirk accepted a voluntary reduction to the permanent rank of Captain for this mission ever been made official. Between 2271 and 2284, therefore, the details of Kirk's career are officially unknown (these dates are, themselves, speculative). What is official is that Kirk retired from Starfleet sometime around 2282 and returned to Starfleet, appointed as an Admiral, in 2284 (Star Trek II: The Wrath of Khan) (according to some sources, including the producers of the film, and costume designers, Kirk's rank is Vice Admiral, however as this has never been stated on screen, by strict guidelines of canon all that is known officially is that his rank was Admiral). By 2284, Kirk was in command of Starfleet Academy's training department.

In 2285, Kirk briefly took command of the Enterprise in order to pursue his old enemy, Khan Noonien Singh, and retained de facto command of the vessel following the death of Captain Spock. He was later demoted back to Captain after stealing the Enterprise and sabotaging the USS Excelsior NX-2000 in 2285 in order to revive Spock. Kirk was given control of a new USS Enterprise A. He commanded the ship for several years until the vessel was decommissioned ca. 2293.

With Dr. Carol Marcus, he had a son named David, who was killed by Klingons in 2285. The death of his son enraged Kirk for years to come. While he had always been distrustful and wary of the Klingon race, after David’s death, he held a barely controlled rage toward them, holding them collectively responsible for the death of his son. When Spock, on behalf of his father Sarek, opened negotiations with the Klingon Empire after the Praxis incident and 'volunteered' Kirk to lead the mission, Kirk was enraged. When Spock pointed out that they were dying, his sharp response was “Let them die!”

It was only when the Klingon Chancellor Gorkon, on his deathbed from an assassination by rogue elements of the Klingons and Federation pleading with him to "Don't let it end this way" that Kirk started to realize not all Klingons were responsible for his son's death. He finally started to let go of his hate of the Klingon people. At the same time, Gorkon's daughter forgave the Federation for her own father’s death.

He recorded in his log during the start of this mission that he could never forgive them for the death of his son. This recording was used as evidence against him when a Klingon court convicted him of murdering Klingon Chancellor Gorkon in 2293; he was sentenced to a life term in the prison mines of Rura Penthe but was subsequently rescued and cleared of guilt.

[edit] Death and resurrection

In the Star Trek: The Next Generation film Generations, he was lost (and presumed dead) when the newest USS Enterprise (NCC-1701-B) was damaged by the Nexus, which he entered. In this alternate plane of existence, he was persuaded by Captain Jean-Luc Picard from the year 2371 to return to planet Veridian III and stop Tolian Soran from sacrificing 230 million lives in order for him to reenter the Nexus. During the climax, Kirk was able to retrieve and activate a cloaking control device from a damaged construction span, enabling Picard to sabotage Soran's plans. However, the span collapsed, causing Kirk to fall to his death.

In the original script of Star Trek: Generations, Soran killed Kirk by shooting him in the back. This filmed ending was changed after negative reactions from test audiences. The revised death in the film was still not well received by fans. In introducing the element of a temporality to the Nexus, the scriptwriters had intended for Kirk to be somewhat immortal.

Shortly after Star Trek: Generations, William Shatner and co-writers Judith & Garfield Reeves-Stevens wrote a series of novels taking place after the events in the movie which detail Kirk's resurrection and subsequent life in the 24th century era. Because of the upset of Kirk's less-than-stellar death in "Generations", these novels have been extremely popular with fans and mainstream audiences - often becoming instant best sellers.

In the novel Star Trek: The Return a Romulan ship transports the body of Captain Kirk from Veridian III shortly after the events in Star Trek: Generations. The Romulans, having a vendetta against Kirk, use an "ancient alien technology" (acquired via an 'alliance' with the Borg) to bring him back, turning Kirk into a puppet for the Romulans. Kirk faces off against several characters from Star Trek: The Next Generation before being subdued, and is treated by Mr. Spock and Dr. McCoy, who are still alive in the 24th century, McCoy removing an implant that was killing him and Spock mind-melding with Kirk to remove the Romulans' conditioning from his brain. Kirk meets with Picard once more, and goes on to destroy the Borg homeworld located in the Delta Quadrant, disabling the Collective (albeit temporarily). He is presumed dead in the final explosion, but is transported away at the last second. At some point, it was explained that V'ger was Borg and Spock's mindmeld with V'ger prevented his assimilation.