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Culkin, 42, beat Edward Norton, Guy Pearce and his Succession co-star Jeremy Strong in the category as the 97th awards show got under way in Los Angeles.
He scooped the gong for A Real Pain, the Jesse Eisenberg-directed film about two cousins who go to their grandmother’s home country of Poland to trace their roots.
Culkin, who has also won a Bafta and a Golden Globe for the role, started his speech by hailing his fellow nominee Strong, saying: “I loved your work in The Apprentice.”
Paying tribute to Eisenberg, he said: “Thank you for this movie, you are a genius, I will never say this again, so soak it up.”
Culkin also said that his wife, Jazz Charton, promised him a fourth child if he won an Oscar he said.
The US actor said that she told him “I will give you four (children) when you win an Oscar”.
He added: “I held my hand and you shook it … I brought it up now – I owe you, no pressure, I love you, I am sorry I did this again, let’s get cracking on those kids.”
The event opened with a video showing well-known places in California and the Hollywood Hills sign in what appeared to be a tribute to the Los Angeles wildfires.
It ended saying: “We love LA.”
Wicked star Ariana Grande then launched into The Wizard Of Oz song Somewhere Over The Rainbow, wearing a red dress and ruby slippers.
Her Wicked co-star star Cynthia Erivo then took to the stage to perform Home from The Wiz, a spin-off film of The Wizard Of Oz.
Grande arrived back on stage, and she and Erivo launched into a duet of Defying Gravity from their film Wicked.
US comedian Conan O’Brien, who is hosting this year, kicked off the ceremony with a recreation of a gruesome scene from body horror The Substance, which stars Demi Moore.
During his opening monologue he referenced the controversy surrounding Netflix musical Emilia Perez and actress Karla Sofia Gascon.
O’Brien said if Gascon wanted to tweet about the awards on Sunday, she should “remember my name is Jimmy Kimmel”.
Published: by Radio NewsHub
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