Gillan's early television acting career included guest appearances on several drama series, with her first role being in an episode of Rebus, a role she obtained while still at Italia Conti. Gillan then undertook a two-year stint as a member of the ensemble cast of the sketch comedy series The Kevin Bishop Show, in which she played multiple characters including celebrities such as Katy Perry and Angelina Jolie. Gillan also appeared on TV in a leading role in a horror project entitled The Well, which was broadcast as a series of episodic short films on BBC Two and later as a web series on BBC.co.uk. Part of the BBC's multimedia "switch" programming, the short episodes interconnect with online games that further explore the environments presented in the series.
Gillan portrayed Amy Pond, companion to the Eleventh Doctor, on the British sci-fi series Doctor Who. Before cast in the lead role in May 2009, she previously appeared on Doctor Who in series four episode "The Fires of Pompeii" in the role of a soothsayer. She made her first on-screen appearance as Amy Pond in "The Eleventh Hour" with her cousin Caitlin Blackwood portraying a younger version of the same character. In 2010, she won in the Entertainment category at Young Scot Awards. She appeared in the sixth series in 2011 and the first five episodes of the seventh series in 2012, after which her character and Rory Williams (portrayed by Arthur Darvill) left the series. Gillan reprised her role in the 2013 Christmas special "The Time of the Doctor".
She was cast in comedian Charlie Brooker's TV series A Touch of Cloth, portraying Kerry Newblood. Gillan joined the regular cast of Adult Swim's NTSF:SD:SUV:: for the show's third season in 2013.
In February 2014, Gillan was cast as the lead in Selfie, an American single-camera sitcom for ABC produced by Warner Bros. Television which was greenlit for the 2014–15 US television season. Gillan played a socialite named Eliza Dooley, a modern-day take on Eliza Doolittle, who is obsessed with social media. This was Gillan's first time in the lead role of an American television series. The series was cancelled by ABC on 7 November 2014 after seven episodes; the remaining six episodes were made available on Hulu starting 25 November 2014.
She appeared in the Channel 4 film Stacked.
In August 2011, it was announced that Gillan would star in an indie Scottish romantic comedy called Not Another Happy Ending alongside Emun Elliott. She was selected by director John McKay because he came to know her during the production of We'll Take Manhattan, which he also directed, as "a very bubbly, vibrant, energetic, funny, slightly clumsy person" who was a perfect fit for the character. Filming took place in July 2012, though Elliott was replaced by Stanley Weber. Gillan told journalists that she was happy to be involved in a Scottish production that "isn't about drug use or fighting the English". The film premiered at the Edinburgh International Film Festival in June 2013. In 2012, Gillan appeared in the television film We'll Take Manhattan playing the part of supermodel Jean Shrimpton, which told the story of Shrimpton's relationship with the photographer David Bailey.
Gillan starred in the lead role in the supernatural horror movie Oculus, which was filmed in Alabama and released in April 2014.
In May 2013, Gillan was cast as Nebula in the Marvel superhero science fiction film Guardians of the Galaxy, which was released in August 2014. Gillan had her head shaved bald for the role.
In May 2014, Gillan was cast in the Western film In a Valley of Violence directed by Ti West, opposite John Travolta, Ethan Hawke and Taissa Farmiga. Gillan portrayed Ellen, the older sister to Farmiga's character.
In 2015, Gillan appeared in the drama film The Big Short directed by Adam McKay, alongside Brad Pitt, Christian Bale, Ryan Gosling, Steve Carell and Melissa Leo. She wrote and directed her first short film, Coward, which screened at the 2015 Edinburgh Film Festival, and nominated for several awards. Later in the year she wrote, directed, and starred in another short film called Conventional.
On 2 November 2016, it was announced that Gillan would write, direct and star in her directorial feature film debut with Burbank-based development and production company Mt. Hollywood Films' indie drama project titled Tupperware Party. Set in her home city of Inverness in the Scottish Highlands, filming began in January 2017 and wrapped in the following month. The title of the film was later changed to The Party's Just Beginning.
In 2017, Gillan reprised her role as Nebula in Guardians of the Galaxy Vol. 2, this time becoming a member of the film's eponymous team, and co-starred in The Circle, alongside Emma Watson, Tom Hanks, and John Boyega. The latter film, released in April, was directed and written by James Ponsoldt, and was based on the novel by Dave Eggers. Also in that year, Gillan played the lead female role in Jumanji: Welcome to the Jungle, a sequel to 1995 film Jumanji, starring alongside Dwayne Johnson, Kevin Hart, Jack Black and Nick Jonas. She replayed Nebula in Avengers: Infinity War and Avengers: Endgame, which were filmed back-to-back. Principal photography began in January 2017, at Pinewood Atlanta Studios in Fayette County, Georgia.
In 2011, Gillan made her first theatre appearance playing the role of Shirley in John Osborne's play Inadmissible Evidence along with Douglas Hodge. The play debuted at the Donmar Warehouse on 16 October 2011.
In November 2013, Gillan appeared on Broadway in a play called Time to Act, one of the plays included in "The 24 Hour Plays on Broadway" to benefit the non-profit Urban Arts Partnership.
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