Weaver emerged in the 1970s Australian New Wave through her work in Ozploitation films such as Stork (1971) for which she won AACTA Award for Best Actress in a Leading Role, Alvin Purple (1973), and Petersen (1974).

In following years, Weaver appeared in the films The Five-Year Engagement (2012), Parkland (2013), Magic in the Moonlight (2014), The Disaster Artist (2017), Bird Box (2018), Widows (2018), Poms (2019), Stage Mother (2020), and Father Stu (2022).

[12] In the 1990s and early 2000s, Weaver found it increasingly difficult to gain roles on screen or television and she devoted much of her energy to the Australian stage, starring in plays including A Streetcar Named Desire, Last of the Red Hot Lovers, Death of a Salesman, Reg Cribb's Last Cab to Darwin, and Chekhov's Uncle Vanya alongside Cate Blanchett and Richard Roxburgh in 2010–11.

Weaver made her Hollywood debut with the 2012 comedy The Five-Year Engagement, alongside Emily Blunt and Jason Segel, and starred in Park Chan-Wook's English-language debut, Stoker, alongside fellow Australian actors Nicole Kidman and Mia Wasikowska, and British actor Matthew Goode.

[14] In 2012, Weaver was again nominated for an Academy Award for her role opposite Robert De Niro in the comedy-drama film Silver Linings Playbook.

She made her American television debut guest-starring as a Rebel Wilson' character mother in her short-lived comedy series Super Fun Night.

In 2014, she starred in the adaptation of Richard Alfieri's play Six Dance Lessons in Six Weeks opposite Gena Rowlands,[15] Marjane Satrapi's comedy-horror The Voices, and the romantic comedy Magic in the Moonlight written and directed by Woody Allen.

She returned to Australia appearing in Last Cab to Darwin (2015) and Goldstone (2016) receiving Australian Film Critics Association for Best Supporting Actress.

She returned to Australia with starring role in the Fox Showcase political thriller Secret City (2016–19), and Stan science fiction series Bloom (2019–20).

In 2019, she starred in the Epix thriller Perpetual Grace, LTD (2019) and in 2021 she began appearing in the recurring role as Caroline Warner in the Paramount Network neo-Western series, Yellowstone.

She lived with Phil Davis, a former Sydney crime reporter, Canberra Press Secretary, and executive producer for Mike Willesee, for five years until 1981.