On television, Coolidge has appeared in the sitcoms Joey (2004–2006), The Secret Life of the American Teenager (2008–2012), 2 Broke Girls (2011–2017), and the drama series The Watcher (2022).

She garnered critical acclaim for her role as Tanya McQuoid, an insecure wealthy woman, in the HBO anthology series The White Lotus (2021–2022), winning two Primetime Emmy Awards and a Golden Globe.

[4] During college, Coolidge aspired to be a dramatic actress similar to Meryl Streep, but instead pursued comedic character acting.

[5] As a student at the American Academy of Dramatic Arts, Coolidge worked as a waitress in a restaurant alongside Sandra Bullock, who also aspired to be an actress.

[7] In 1994, she was a regular on She TV, a short-lived sketch comedy that also featured Nick Bakay, Elon Gold, Simbi Khali, and Linda Kash.

In 2003, she played the protagonist's agent Luise in Testosterone filmed in Argentina starring David Sutcliffe as Dean Seagrave and Antonio Sabato, Jr., as Pablo.

In 2004, she had a supporting role in the romantic comedy A Cinderella Story playing Hilary Duff's character's vain, self-absorbed stepmother.

[16] In 2003, she starred in an episode of Friends in its final season as Amanda, an obnoxious acquaintance whom Phoebe Buffay and Monica Geller try to shake off.

[17][18] Coolidge also appeared in 1998 in the children's comedy Slappy and the Stinkers, and as the voice of Aunt Fanny in the animated feature Robots in 2005.

[21] In 2006, she guest starred on an episode of Top Chef, and played Adam Sandler's wife's friend, Janine, in the comedy film Click.

From 2000 to 2006 she played comic parts in the improv mockumentaries Best in Show, A Mighty Wind, and For Your Consideration, all directed by Christopher Guest.

[23] However, Variety did praise Coolidge for providing a few bright moments with a spot-on spoof of Streisand, albeit otherwise unimpressed describing the film as "padded and repetitious".

A. O. Scott of The New York Times called the film "irreverent and also appreciative, dragging its satiric prey down to the lowest pop-cultural denominator" and added, "The humor is coarse and occasionally funny.

[27] Also In 2009, she starred alongside Heather Graham and Amber Heard in ExTerminators, a black comedy about a set of women who form their own "silent revolution", wreaking havoc on the abusive men in their lives.

[33] In October 2011, Coolidge began a recurring role in the CBS sitcom 2 Broke Girls as Zofia "Sophie" Kaczyński, a Polish neighbor of the two lead characters.

In 2020, she starred in Like a Boss, the first studio comedy film of the 2020s, for Paramount Pictures, co-starring with Tiffany Haddish, Rose Byrne, and Salma Hayek.

[44] Coolidge had a supporting role in Emerald Fennell's directorial debut Promising Young Woman as the mother of Carey Mulligan's character, Cassie.

The show premiered in July 2021 and was widely praised, with Coolidge receiving critical acclaim and winning a Primetime Emmy Award for Outstanding Supporting Actress in a Limited or Anthology Series or Movie for her performance.

[48] In 2021, she starred in the Netflix Christmas romantic comedy Single All the Way alongside Michael Urie, Philemon Chambers, and Kathy Najimy.