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Neil's first film was a New Zealand television movie The City of No (1971). He followed it with a short, The Water Cycle (1972) and the TV movie Hunt's Duffer (1973). Neill wrote and directed a film for the New Zealand National Film Unit, Telephone Etiquette (1974). He also appeared in Landfall (1976).
Neill's breakthrough performance in New Zealand was the film Sleeping Dogs (1977), the first local film to be widely screened abroad.
Neill went to Australia where he had a guest role on the TV show The Sullivans. He was the romantic male lead in My Brilliant Career (1979), opposite Judy Davis, which was a big international success.
He made some Australian films that were less widely seen: The Journalist (1979), Just Out of Reach (1979) and Attack Force Z (1981), and appeared in television productions such as Young Ramsay and Lucinda Brayford.
In 1981, he won his first big international role, as Damien Thorn, son of the devil, in Omen III: The Final Conflict; also in that year, he played an outstanding main role in Andrzej Żuławski's cult film Possession.
He was one of the leading candidates to succeed Roger Moore in the role of James Bond, but lost out to Timothy Dalton. Among his many Australian roles is playing Michael Chamberlain in Evil Angels (1988) (released as A Cry in the Dark outside of Australia and New Zealand), a film about the case of Azaria Chamberlain.
Neill has played heroes and occasionally villains in a succession of film and television dramas and comedies. In the UK, he won early fame and was Golden Globe nominated after portraying real-life spy, Sidney Reilly, in the mini-series Reilly, Ace of Spies (1983). An early American starring role was in 1987's Amerika, playing a senior KGB officer leading the occupation and division of a defeated United States. His leading and co-starring roles in films include the thriller Dead Calm (1989), the two-part historical epic La Révolution française (1989) (as Marquis de Lafayette), The Hunt for Red October (1990), Death in Brunswick (1990), Jurassic Park (1993), Sirens (1994), The Jungle Book (1994), John Carpenter's In the Mouth of Madness (1995), Event Horizon (1997), Bicentennial Man (1999), the comedy The Dish (2000), and Jurassic Park III (2001).
Neill has occasionally acted in New Zealand films, including The Piano (1993), Perfect Strangers (2003), Under the Mountain (2009), and Hunt for the Wilderpeople (2016). He returned to directing in 1995 with the documentary Cinema of Unease: A Personal Journey by Sam Neill (1995) which he wrote and directed with Judy Rymer.
In 1993, he co-starred with Anne Archer in Question of Faith, an independent drama based on a true story about one woman's fight to beat cancer and have a baby. In 2000, he provided the voice of Sam Sawnoff in The Magic Pudding. In 2001, he hosted and narrated a documentary series for the BBC entitled Space (Hyperspace in the United States).
He portrayed the eponymous wizard in Merlin (1998), a miniseries based on the legends of King Arthur. He reprised his role in the sequel, Merlin's Apprentice (2006).
Neill starred in the historical drama The Tudors, playing Cardinal Thomas Wolsey. "I have to say I really enjoyed making The Tudors", he said, "It was six months with a character that I found immensely intriguing, with a cast that I liked very much and with a story I found very compelling. It has elements that are hard to beat: revenge and betrayal, lust and treason, all the things that make for good stories."
He acted in the short-lived Fox TV series Alcatraz (2012) as Emerson Hauser. He played the role of Otto Luger in the fantasy adventure movie The Adventurer: The Curse of the Midas Box (2014). He had a role in the BBC series Peaky Blinders, set in post-World War I Birmingham. He played the role of Chief Inspector Chester Campbell, a sadistic corrupt policeman, who came to clean up the town on Churchill's orders. In the 2015 BBC TV miniseries And Then There Were None, based on Agatha Christie's thriller, he played the role of General MacArthur.
In 2016, he starred in the New Zealand-made film, Hunt for the Wilderpeople, directed by Taika Waititi, as well as the ITV miniseries Tutankhamun. In 2017, Neill appeared in a scene in Waititi's fantasy sequel Thor: Ragnarok, in which he portrays an actor playing Odin (as depicted by Anthony Hopkins), alongside Luke Hemsworth and Matt Damon as actors playing Thor and Loki, respectively. He portrays the same actor in Thor: Love and Thunder in 2022.
In 2018, he portrayed Mr. McGregor and also provided the voice of Tommy Brock, in Peter Rabbit. In 2019, he was cast for the role of Denis Goldberg in Escape from Pretoria; however, the role was subsequently recast with Ian Hart. In late 2019, he was announced to reprise his character of Dr. Alan Grant in Jurassic World Dominion, which released in July 2022.