[4] In 2003, Havill played Group Captain Windbreak in Justin Butcher's production of The Madness of George Dubya at the Arts Theatre in London.
Michael Billington wrote in The Guardian that "Butcher's production... has a surprising jauntiness; ... Andrew Havill as an ineffectual group captain... stand[s] out.
"[7] The following year, Havill was cast as the Reverend James Morell in George Bernard Shaw's Candida, for which The Guardian's Lyn Gardner wrote "Much of the pleasure of Christopher Luscombe's well-observed period production is in watching Andrew Havill's interesting Morell move from confident self-belief to bewildered self-doubt as he starts to understand that even goodness is a form of selfishness.
Ben Brantley commented in The New York Times, "As Ford... the excellent Mr. Havill is exactly as serious as he needs to be, reminding us that one of comedy’s main functions is to defuse bombs that in real life often explode and destroy.
In 2012, he was cast as the Royal Equerry, Harry, in the episode A Scandal in Belgravia of the mystery crime drama Sherlock due to his reputation for playing "well-spoken upper-class types.
He and twelve other cast members were nominated for the Screen Actors Guild Award for Outstanding Performance by an Ensemble in a Drama Series for their roles in The Crown.
[25] In 2024, he portrayed the criminal defence lawyer Stuart Wentworth QC in the British television drama Mr Bates vs The Post Office.
[29] He played the cabinet secretary to Meryl Streep's Margaret Thatcher in The Iron Lady (2011), Cameron in Hyde Park on Hudson (2012), and Turing's professor in The Imitation Game (2014).
[6] His work of the 2010s includes roles in The Awakening as George Vandermeer, Cloud Atlas as Mr. Hotchkiss, Dad's Army as Captain Meeks, My Cousin Rachel as Parson Pascoe, Gold as Sir James Benson, and Lyrebird as Maarten Wooning.
[21] Havill portrayed Sir Philip Hendy in Roger Michell's 2020 film The Duke, along with actors Jim Broadbent and Helen Mirren.