Waterston's first starring role on film was in the 2007 independent drama
The Babysitters, alongside
John Leguizamo and
Cynthia Nixon. Also in 2007, Waterston performed in the play
Los Angeles by Julian Sheppard. The following year, she acted in
Kindness, a play by
Adam Rapp. In 2010, Waterston played Gena in the original Off-Broadway production of
Leslye Headland's
Bachelorette, the role played by
Lizzy Caplan in the
2011 film version. In 2011, she played Anya in the
Classic Stage Company revival of
The Cherry Orchard. Also in 2011, she performed in Rapp's
Dreams of Flying, Dreams of Falling at the
Classic Stage Company. After supporting roles in films including
Enter Nowhere (2011),
Being Flynn (2012),
The Letter (2012) and
The Disappearance of Eleanor Rigby (2013), Waterston was cast in the 2014 crime film
Inherent Vice, written and directed by
Paul Thomas Anderson. The film and her performance received generally positive reviews from critics. The following year, she appeared in
Queen of Earth and played
Chrisann Brennan in director
Danny Boyle's biographical drama
Steve Jobs, starring
Michael Fassbender. In 2016, Waterston was cast as
Tina Goldstein in the fantasy film
Fantastic Beasts and Where to Find Them opposite
Eddie Redmayne. The film received generally positive reviews from critics and became a commercial success, grossing $814 million worldwide. Waterston reprised her role in
Fantastic Beasts: The Crimes of Grindelwald in 2018, and had a short part in
Fantastic Beasts: The Secrets of Dumbledore (2022). In 2017, she starred alongside Fassbender for director
Ridley Scott in the science fiction horror film
Alien: Covenant. That year she also starred in
Steven Soderbergh's comedy-drama
Logan Lucky and
Alfonso Gomez-Rejon's historical drama
The Current War. Waterston's next starring roles were in the independent films
State Like Sleep (2018),
Mid90s (2018),
Amundsen (2019) and
The World to Come (2020). In 2020, she starred in the British-American horror drama series
The Third Day alongside
Jude Law. In 2022, she joined the cast of the second season of
HBO period drama series
Perry Mason. ==Personal life==