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She started her acting career in 1974 as a cast member of The Second City in Toronto. She was an understudy for Gilda Radner until she left for Saturday Night Live. Two years later, this theatre troupe created the television series SCTV, on which she became a regular performer. Memorable O'Hara characterizations on the show included Las Vegas scorcher (I wanna bear your children!) Lola Heatherton, buzzer-happy game show contestant Margaret Meehan, raunchy nightclub comedian Dusty Towne, soap opera seductress Sue Ellen and stage actress Sue Bopper Simpson.

In the late 1970s, she did various voice-overs for a number of cartoons, which would continue throughout her career. During a short time in the early 80's when SCTV was in between network deals, she was hired to replace Ann Risley when Saturday Night Live was being retooled in 1981. However, she quit the show without ever having made an appearance on it, choosing to go back to SCTV when the show signed on with NBC and was back on the air. Her SNL position was then given to fellow Canadian Robin Duke, who had also replaced O'Hara for a season on SCTV.

She had roles in many films over the years, including Martin Scorsese's After Hours in 1985, as well as parts in two Tim Burton films, Beetlejuice and The Nightmare Before Christmas. She played Kate McCallister in the first two Home Alone films. In 2006, she starred in her fourth Christopher Guest film, For Your Consideration (following Waiting for Guffman, Best in Show, and A Mighty Wind).

On June 9, 2007, she was inducted into Canada's Walk of Fame. In May 2008, it was announced that she has signed on to star in the upcoming ABC dramedy Good Behavior.

O'Hara was born in Toronto, Ontario to a large Irish Catholic family. A naturalized U.S. citizen, she married production designer/director Bo Welch in 1992 and has two sons, Matthew (b.1994) and Luke (b.1997). She is the sister of critically-acclaimed singer-songwriter Mary Margaret O'Hara, though she is a singer-songwriter in her own right, having written and performed songs in the 2003 film A Mighty Wind. She has a condition known as Dextrocardia with situs inversus.