• James T. Kirk: William Shatner
• Spock: Leonard Nimoy
• Leonard "Bones" McCoy: Deforest Kelley
• Chekov: Walter Koenig
• Sulu: George Takei
• Uhura: Nichelle Nichols
• Dr. Gillian Taylor: Catherine Hicks
• Klingon Ambassador: John Shuck
• Admiral Cartwright: Brock Peters
• Amanda (Spock's Mother): Jane Wyatt
• Majel Barret: Christine Chapel

An enormous alien probe on a heading for Earth encounters and completely cripples the USS Saratoga, continuing unchecked toward Earth, where a high-ranking Klingon Ambassador is trying to convince the Federation Council that the Genesis device was, in fact, a weapon designed to eradicate the Klingon species. The Ambassador promises that there will be no peace between the Klingons and Federation while Kirk lives.

In the meantime, Kirk and the rest of his crew, excluding Saavik, who stays behind, leave Vulcan in their hijacked Bird of Prey, which McCoy has renamed the "Bounty". While en route to Earth, they receive an emergency transmission informing them that Earth's defenses have been neutralized by a huge vessel of unknown origin, and that the alien ship is beginning to destroy the atmosphere and oceans, all the time transmitting indecipherable sounds. Analyzing a recording of the sounds transmitted by the alien ship, Spock determines that the probe can not be responded to because the sounds are apparently analogous to songs sung by humpback whales - extinct in the 23rd century. Kirk decides to risk a slingshot around the sun to send the Bounty into a time warp to Earth of the past and bring back enough whales to repopulate the species and, more importantly, respond to the probe.

The Bounty lands in San Francisco, 1986, and the crew splits into three teams. Kirk and a thinly disguised Spock set out to find the whales, which Kirk decides to take from the Cetacean Institute, a museum devoted to whales. There, Kirk meets Dr. Gillian Taylor as she leads a tour of the Institute, during which she shows off the Institute's two whales, George and Gracie. Gillian also reveals that the whales will have to be released into the open sea due to the cost of keeping them in captivity. Spock dives into the whale tank and mind-melds with one of the whales, finding that Gracie is pregnant, but Gillian throws them out of the Institute, only to find them walking back to Golden Gate Park and picks them up again.

Chekov and Uhura find the Navy's USS Enterprise and sneak in to collect photon spillage from the ship's nuclear reactor in order to replenish the dilithium crystals on the Bounty for the return trip to the 23rd century, while Scotty, Sulu and McCoy seek out the materials necessary to build a tank for the whales and their water in the Bounty. Scotty's team visits a Plexiglas factory, where he trades the "recipe" for transparent aluminum (common in the 23rd century) in for the necessary materials and the loan of a helicopter to return the tank walls to the Bounty. (Scotty insists no damage is being done to history - perhaps the director of the factory to whom Scotty revealed the "secret" is the inventor!)

Uhura and Chekov gather the necessary energy to ready the Bounty for its next time warp, but they are detected on the carrier. Chekov gives Uhura the collection device and has her beamed back to the Bounty, while he is captured and briefly interrogated. Chekov escapes again, but is seriously wounded and taken to a hospital.

Kirk, having befriended Gillian and learned how upset she is that "her" whales are about to be turned loose, gets the frequency to radio tags that the whales will be carrying so scientists can track them, but even Gillian doesn't know the exact location to which the whales will be taken. Kirk receives the news of Chekov's injury and, with McCoy, mounts a rescue operation which will require the help of Gillian. They enter the hospital disguised as surgeons, and McCoy performs a quick fix returning Chekov to normal after expressing alarm that 20th century medicine would have called for a hole to be drilled into Chekov's skull. They "kidnap" Chekov from the hospital and take him back to the Bounty, where Gillian stows away by jumping Kirk just as he is beamed aboard. The Bounty lifts off and reaches the whales' coordinates in the Pacific, only to find a whaling ship is in hot pursuit of George and Gracie. Kirk orders the Bounty to decloak, which frightens the poachers away while the two whales are beamed aboard. The Bounty makes it back to the 23rd century and crash-lands in San Francisco Bay after being disabled by the probe, and Kirk releases the whales into the ocean. George and Gracie re-establish contact between Earth's whales and the aliens - a dialogue which had been in progress before man even existed - and Gillian begins her new life as a Federation cetacean biology specialist. Kirk and the others are exonerated for all charges against them concerning the theft and destruction of the starship Enterprise, except for Kirk, who is demoted to Captain and given command of a new, more advanced vessel: the new Enterprise, NCC-1701-A.