[12] Ronan made her screen debut on Irish national broadcaster RTÉ, in the 2003 prime time medical drama The Clinic and appeared in the mini-serial Proof.

[13] During the same time, Ronan auditioned for the part of Luna Lovegood in the fantasy film Harry Potter and the Order of the Phoenix (2007), a role she lost out to fellow Irish actress Evanna Lynch.

She auditioned for and won the part of Briony Tallis, a 13-year-old aspiring novelist, who affects several lives by accusing her sister's lover of a crime he did not commit.

[18] Ty Burr of The Boston Globe called her "remarkable [and] eccentric",[19] and Christopher Orr of The Atlantic wrote that she is "a marvel, elegantly capturing the narcissism and self-doubt that adhere to precocity".

[23] In 2009, Ronan starred alongside Rachel Weisz, Mark Wahlberg, Susan Sarandon and Stanley Tucci in Peter Jackson's supernatural drama The Lovely Bones, an adaptation of the book of the same name by Alice Sebold.

Ronan played 14-year-old Susie Salmon, who, after being raped and murdered, watches from the after-life as her family struggles to move on with their lives while she comes to terms with her quest for vengeance.

[26] Reviewers were critical of the film's story and message,[27] but Richard Corliss of Time believed that Ronan had successfully invested the gruesome tale with "immense gravity and grace".

[29] Sukhdev Sandhu of The Daily Telegraph considered Ronan to be the sole positive aspect of the production, writing that she "is simultaneously playful and solemn, youthful yet old beyond her years".

[32] The following year, Ronan reunited with Joe Wright to play the title character in the action film Hanna, about a 15-year-old girl raised in the Arctic wilderness to be an assassin.

[34] In his review for Rolling Stone, Peter Travers termed the film "a surreal fable of blood and regret" and labelled Ronan an "acting sorceress".

[40] Peter Jackson approached Ronan to play an elf in The Hobbit film series, but she withdrew from the project due to scheduling conflicts.

[41] She was instead drawn to Neil Jordan's horror film Byzantium (2012), as the "dark, gothic and twisted" project provided her an opportunity to play a more complex and mature character.

[42] Writing for Radio Times, the critic Alan Jones found the film to be an "evocative fairy tale that uses vampires as a prism to comment on humanity" and considered both Arterton and Ronan to be "radiant" in it.

[43] In a 2013 film adaptation of Stephenie Meyer's novel The Host, Ronan played the dual role of Melanie Stryder, a human rebel, and Wanderer, a parasitic alien.

Critics disliked the film;[44] Manohla Dargis termed it "a brazen combination of unoriginal science-fiction themes [and] young-adult pandering", but took note of an "otherworldly aspect to [Ronan's] screen presence, partly due to her stillness and her own translucent eyes, which can suggest grave intensity or utter detachment".

[57] In 2016, Ronan moved to New York City to begin rehearsals for her debut appearance on Broadway, in a revival of Arthur Miller's play The Crucible.

[62] Writing for The Hollywood Reporter, David Rooney considered Ronan to be "icy and commanding" and Linda Winer of Newsday commented that she had played the part "with the duplicity of a malevolent surfer-girl".

[63] Ronan next voiced Marguerite Gachet in the biographical animated drama Loving Vincent (2017), and starred alongside Billy Howle as troubled newlyweds on their honeymoon in a film adaptation of Ian McEwan's novel On Chesil Beach.

[70] In a mixed review of the film, Michael O'Sullivan of The Washington Post praised Ronan's performance, writing that she "makes for an incandescent Nina, especially in her loopy final-act speech".

[73] Critic Todd McCarthy praised both actresses' performances and credited Ronan for "carr[ying] the film with fiercely individualistic spirit".

[74] After becoming aware of a forthcoming film adaptation of Louisa May Alcott's novel Little Women, written and directed by Greta Gerwig, Ronan campaigned to play the lead role of Jo March, an aspiring author in the American Civil War era.

[75] In preparation, she read Marmee & Louisa, a biography about Alcott and her mother; the cast rehearsed the script for two weeks, and filming took place on location in Concord, Massachusetts.

[77] Richard Lawson of Vanity Fair took note of how well Ronan had portrayed her character "in all her conflicted loyalty, the struggle between her familial contentment and her yearning for something more".

[81] In 2020, Ronan portrayed the geologist Charlotte Murchison opposite Kate Winslet's Mary Anning in Francis Lee's Ammonite, a drama about a romantic relationship between the two women in the 1840s.

[85] Alexandra Pollard of The Independent took note of Ronan's "rare skill to make Shakespeare’s beautiful but weighty words easy to understand".

[88] She then starred opposite Paul Mescal in a 2023 film adaptation of the science fiction novel Foe by Iain Reid, directed by Garth Davis.

[93] Ronan also starred in the film as Rona (based on Liptrot); she found playing her character's struggle with alcoholism to be "very upsetting" as she had personally experienced the effects of addiction from those close to her.

[100] Ronan will next lead the comic thriller Bad Apples, playing a primary school teacher disrupted by an unruly student.

[113] She joined Twitter in late 2009 due to being a fan of English comedian Stephen Fry, whose prolific usage of the platform has been well documented, but soon deleted her account.

[119] Erica Wagner of Harper's Bazaar has described Ronan's off-screen persona as "lively, funny, warm", while Vanessa Thorpe of The Guardian found her "unpretentious".