Chakotay was born on a colony world that his tribe had moved to a number of years earlier, in what would become the Demilitarized Zone between the Federation and the Cardassian Empire. As a young man he decided to apply to Starfleet Academy, and was sponsored by Captain Sulu. He graduated from the academy in 2348 and was commissioned as a Starfleet Officer.
In the 2360s the Cardassians began harassing the colonists living along their border, in the hopes of forcing them to leave so they could claim the worlds for themselves. Feeling abandoned by the Federation, the colonists formed the Maquis. Kolopak had joined the Maquis as he felt his tribe could not abandon their world to the Cardassians. When Kolopak was killed Chakotay resigned from Starfleet and returned home to help his people keep their homes.
Chakotay and his crew were swept in to the Delta Quadrant, along with the USS Voyager which was sent after them. When Voyager became trapped in the Delta Quadrant Chakotay and his crew joined with the Starfleet crew on Voyager to increase their chances of survival and returning to the Alpha Quadrant. Chakotay became first officer on the Voyager under Captain Kathryn Janeway.
At first relations between the Starfleet and former Maquis crew were strained, with Chakotay making it clear to Janeway he would not be her "Token Maquis" on the journey home. Before too long the crew began to bond together in the face of many trials. Janeway and Chakotay became close friends during their time in the Delta Quadrant. By the time contact with Starfleet was re-established in 2374 Janeway and Chakotay thought of the Voyager crew as a single, unified crew.
In 2378 Voyager returned to the Alpha Quadrant. Chakotay and the other former Maquis members were pardoned for their activities as Maquis members under the blanket pardon given to the Maquis who had returned to Starfleet during the Dominion War.
Even though some of the brass was still suspicious of Chakotay, he was promoted to Captain of Voyager after Janeway was promoted to Admiral and reassigned to Starfleet Command. After the Borg invasion of 2381 Chakotay was assigned to the Project Full Circle fleet, commanding Voyager as she returned to the Delta Quadrant.
- It was not made clear as to whether Chakotay was referring to Hikaru Sulu, Demora Sulu, or another Sulu entirely when he told his father about Sulu sponsoring him for the academy. The novel Pathways stated that the Sulu in question was Demora's son Hiromi Sulu. The short story Seduced stated that it was Demora who sponsored him, and that Chakotay had lied about Sulu's gender to his father.