He began a collaboration with dramatist Kenneth Lonergan in 2002, starring as multiple characters in the West End and Broadway productions of the play This Is Our Youth.

His role as a free-spirited drifter in Jesse Eisenberg's comedy-drama film A Real Pain (2024) earned him a nomination for the Academy Award for Best Supporting Actor.

[2] He was the fourth of seven children born to Christopher "Kit" Culkin, a former stage actor, and Patricia Brentrup, a native of North Dakota.

"[12] Because his father served as a sacristan at the St. Joseph's Church of Yorkville, Culkin attended its Catholic school for free until the third grade.

[4] His career began when a neighbor, a stage manager who worked for the repertory theatre Light Opera of Manhattan, heard the company needed some children for a production.

[4] His first professional gig was through a television commercial based on learning disabilities;[21] he was repeatedly berated by the unnamed director in a failed attempt to make him method act.

[24] Home Alone was originally met with mixed-to-positive reviews from critics;[26] Culkin's small role was deemed memorable for its Pepsi product placement.

In 1996, he starred as a farm boy who overcomes his fear of animals in Bobby Roth's Amanda and was a guest caller on the fourth season of the television sitcom Frasier.

[48] He appeared in two feature directorial debuts the following year: Peter Care's The Dangerous Lives of Altar Boys as a mischievous Catholic schoolboy and Burr Steers's Igby Goes Down as the rebellious and sardonic teenager Jason "Igby" Slocumb Jr.[49][50] Film critic Stephen Holden for The New York Times praised both comedy-dramas,[51] but found Culkin's breakthrough performance in the latter to be "even richer" than the former.

[56] As he needed time to figure out whether he genuinely wanted to be an actor or not, he took a break from the film and television industries and only focused on the acting jobs that interested him the most.

[59] In 2006, Culkin starred in Eric Bogosian's off-Broadway revival of SubUrbia,[60] and made his on-Broadway debut by appearing in Julia Cho's one-act play First Tree in Antarctica.

[20] Culkin made his intermittent return to the screen with Derick Martini's Lymelife (2008), a teen comedy film executive produced by Martin Scorsese.

[67] In Edgar Wright's action comedy Scott Pilgrim vs. the World (2010), Culkin portrayed the titular character's "cool gay roommate" Wallace Wells.

[69][70] Culkin played a small role in Lonergan's psychological drama Margaret (2011),[71] before starring in the critically panned comedies Movie 43 (2013) and Quitters (2015).

[75] Culkin recalled feeling comfortable with acting while he was filming the science fiction comedy Infinity Baby (2017), and began settling into it being something he would do for a living.

[76] From 2018 to 2023, Culkin received renewed recognition from mainstream audiences for his lead role as Roman Roy, the immature and irresponsible media executive, in the HBO black comedy-drama series Succession.

[83] He played a supporting role in Steven Soderbergh's crime thriller No Sudden Move (2021),[84] and hosted the November 6, 2021 episode of the variety series Saturday Night Live; marking thirty years since his brother Macaulay anchored.

[85] In 2022, Culkin narrated the documentary miniseries Gaming Wall Street and joined the adult animated sitcom Solar Opposites as a main character.

Owen Gleiberman of Variety called it a "sensational piece of acting,"[91] while The Washington Post's Ty Burr found it "both liberating and touched by a deeper, more inarticulate sadness.

[93][94][95][96] Culkin will next return to the stage as Richard Roma in Patrick Marber's Broadway revival of Glengarry Glen Ross, opposite Bob Odenkirk and Bill Burr.

[99] During his parent's separation and subsequent custody battle in 1995, a 13-year-old Culkin delivered a handwritten note to the New York Supreme Court requesting to bar the media from entering the courtroom.

[115] Culkin declined to speak about his relationship with Jackson in the wake of the documentary film Leaving Neverland (2019), due to its sensitive nature.

[116] According to the review-aggregation website Rotten Tomatoes, Culkin's most critically acclaimed films include The Mighty (1998), The Cider House Rules (1999), The Dangerous Lives of Altar Boys (2002), Igby Goes Down (2002), Scott Pilgrim vs. the World (2010), Weiner-Dog (2016), Infinity Baby (2017), No Sudden Move (2021), and A Real Pain (2024).