After eighteen months of modeling, she studied acting with Kate McGregor Stewart while still modeling on the side. Her first major roles were in the short-lived 1983 television series Paper Dolls playing a model and in the feature film Back to School with Rodney Dangerfield. In the spring of 1989, she began studying acting with Stella Adler and appeared in a number of guest-starring roles in series like Quantum Leap and The Cosby Show. In 1992, she played Cat in a second pilot for a U.S. version of Red Dwarf, which was not picked up.

A year later, she was offered a lead role in Star Trek: Deep Space Nine: Farrell starred as Jadzia Dax, Deep Space Nine's Starfleet science officer; a character who is host to a 300-year-old symbiont and can draw upon the memories and knowledge of the symbiont's six previous hosts. She left the show at the end of the sixth season; as a result, Paramount Pictures decided to kill off Farrell's character.

Farrell then co-starred on Paramount's