[13] After graduating high school, Lynskey studied for a year and a half at Victoria University of Wellington, majoring in English literature,[14] but dropped out to focus on her film career.

[34] Her return to substantial film roles came with the independent drama Foreign Correspondents, where she played Melody, a timid receptionist who strikes up an unusual bond with an overseas pen pal.

[36] Her next film was the period fairytale romance Ever After (1998), a feminist reimagining of Cinderella that was shot in the south of France;[38][39] Lynskey played Drew Barrymore's "charming and funny" stepsister, Jacqueline De Ghent.

[42][43][44] Next, she wore "big hair and fake nails" to portray Gloria,[45] a girl from New Jersey, in the musical romantic comedy Coyote Ugly (2000), with Salon's Stephanie Zacharek calling her "a bridge-and-tunnel Betty Boop, full of google-eyed charm".

[49] In 2002, Lynskey re-teamed with director Andy Tennant—whom she previously worked with on Ever After—to play a key role in the romantic comedy Sweet Home Alabama, with The Austin Chronicle mentioning her as a highlight among the ensemble cast.

Critic Andrew Sarris noted that "the performances [of] Ms. Sevigny, Ms. Dawson and Ms. Lynskey do more than [just] complement Mr. Christensen's central characterization; they provide a sane backdrop for [his] pathological deceptions to steadily unravel against".

[55] Worried about being typecast as a result of her involvement with the series,[56] Lynskey decided to leave the main ensemble in 2005 to concentrate on film work, a move that showrunner Chuck Lorre said he had "a lot of respect for", despite "not [being] happy at first".

[60] She then joined the main ensemble of the short-lived Fox series Drive (2007),[61] with Los Angeles Times critic Mary McNamara describing her work as Wendy Patrakas, a new mother desperate to get away from her abusive husband, as "especially compelling".

[63] Later that year, she returned once again to New Zealand to headline the romantic drama Show of Hands,[64] earning strong notices and a Best Actress nomination at the Qantas Film Awards for playing Jess, a single parent who enters a gruelling endurance competition to win a car.

"[71] She co-starred that same year as Ginger, the foolishly devoted wife of thieving whistleblower Matt Damon's Mark Whitacre, in Steven Soderbergh's darkly comedic biopic The Informant!.

[57] Also in 2009, Lynskey appeared as the pregnant girlfriend of a cannabis farmer in Tim Blake Nelson's Leaves of Grass, with RogerEbert.com believing her performance to be one of the key contributors to the black comedy's "quirky charm".

"[90] In 2012, Lynskey appeared briefly as the flirtatious Karen in doomsday romantic comedy Seeking a Friend for the End of the World and had a key role as Aunt Helen, the sexually abusive relative of the teenage protagonist, in the coming-of-age drama The Perks of Being a Wallflower.

[93] In their critique of the film, the Tallahassee Democrat stated that Lynskey "steals the show ... [Putzel] sparks to life whenever [she] arrives on the screen",[94] while Redefine described her as "delightful" and "deftly believable".

The film drew attention for being almost entirely improvised,[107] with Stephen Holden of The New York Times stating, "The performances [are] so natural that the actors melt into their characters";[108] while other critics singled out Lynskey as a highlight.

[120][121] Writing for the Los Angeles Times, Robert Lloyd said, "[Lynskey] is all deep waters and live wires; soft and steely, trying on new personas for size, her Michelle becomes the series' gravitational center.

[132] She sought the help of a therapist before the film went into production to prepare herself for working with DuVall, a close friend of several years: "I didn't want anything to happen to our friendship and a big challenge was being able to stick up for myself and my perspective in regard to the script and this character.

A performance like this one can be quite tricky—you're essentially reactive a lot of the time, more of a sponge for the film than the motor driving it along—but Lynskey makes everything active by letting you feel Ruth's emotions and sense her train of thought as she puts various pieces together in her head, drawing correct or wrongheaded conclusions.

[141]I Don't Feel at Home won the Grand Jury Prize at the 2017 Sundance Festival while Lynskey received a nomination for that year's Gotham Independent Film Award for Best Actress.

[145] That same year, she received a Golden Nymph nomination for starring as Zara Skelton, a headstrong criminal defence lawyer, in the Australian miniseries Sunshine;[146] played the mother of a teenage witch in The Changeover, a fantasy thriller shot in New Zealand;[147] and appeared as a flustered housewife—frantically trying to conceal her husband's corpse after finding him dead—in the horror film XX.

Variety described her work in the drama as "compelling",[149] while Frank Scheck of The Hollywood Reporter stated, "It's no surprise that Lynskey, who has quietly [been] establishing herself as one of indie cinema's finest actors, is once again superb in her emotionally complex turn".

[150] Next, she appeared in the principal role of troubled psychic Molly Strand on the first season of Castle Rock, a supernatural horror series based on characters and settings from the books of Stephen King.

[154] Between April and May 2020, Lynskey appeared as Rosemary Thomson in the FX on Hulu period miniseries Mrs. America, a political drama centred on the life and career of conservative activist Phyllis Schlafly (played by Cate Blanchett).

[158] Lynskey agreed to star as a layabout stoner in Lady of the Manor (2021), the directorial debut of Justin Long, because "the thought of being in sweatpants [and] acting like I was high for a whole movie was so freeing".

[161] Adam McKay's satirical tackling of the climate crisis, Don't Look Up, was Lynskey's second film project that year: her portrayal of June Mindy, Leonardo DiCaprio's put-upon wife, was described as "terrific" by The Hollywood Reporter,[162] while IndieWire called her "low-key brilliant" and felt she brought a "clear-headed" presence to the narrative.

[167] For her work on Yellowjackets, Lynskey won Best Actress in a Drama Series at the 27th Critics' Choice Awards, where her acceptance speech drew attention for paying tribute to her daughter's nanny.

Airing on Hulu in May 2022, the show's acting was widely praised: Entertainment Weekly felt that Lynskey "captures the sadness and seething resentment of a woman stifled by the confines of stay-at-home motherhood",[172] while RogerEbert.com's Brian Tallerico said, "She does so much with just a sigh or defeated body language.

[171] In the Peacock historical drama series The Tattooist of Auschwitz, Lynskey portrayed New Zealand social worker Heather Morris, a fledgling novelist who befriends an elderly Holocaust survivor, played by Harvey Keitel, and pitches him her idea for a book about his time spent imprisoned at a concentration camp.

The show was released in May 2024, with The Daily Beast's Nick Schager pointing out Lynskey's chemistry with Keitel but criticising the quality of the wig she had to wear in an effort to resemble the real Morris.

The event was directed by Jason Reitman, who assembled a cast of women to read the all-male script; Lynskey played the role of George Aaronow, originally portrayed by Alan Arkin.

[215] That same year, when asked how she was dealing with the response to her role on Yellowjackets, Lynskey explained to The Guardian that a lot of attention was being placed on her weight: "It's [about] trying to tune out [the negative comments] and [listening instead] to the women who say: thank you for just being on screen and not pinching your tummy, or being like: 'I wish I was thinner'".