Celia's varied career spans films, television and radio drama, and the theatre. Her film credits include Nanny McPhee, Hilary and Jackie (playing Iris du Pré) and the 1997 film of The Borrowers where she played Homily Clock. Other films include Bridget Jones's Diary, Calendar Girls, Highlander and, as Fighter Pilot Bravo 5, in Star Wars Episode I: The Phantom Menace. In 2004, Imrie played Doctor Imogen Reed in the schoolgirl thriller, Out of Bounds. She appeared in St Trinian's in 2007 as the Matron, alongside Stephen Fry, Rupert Everett, Colin Firth, Russell Brand and Mischa Barton.
Television series to feature Imrie include The Nightmare Man, Bergerac, Oranges Are Not the Only Fruit, Absolutely Fabulous, The Darling Buds of May and Upstairs, Downstairs. In the 2000 miniseries of Gormenghast, she played Lady Gertrude. She also had a guest appearance in an episode of the BBC Scotland sitcom Still Game in 2003, where she played a home help called Mrs Begg. She also appeared in the 2005 BBC television drama Mr. Harvey Lights a Candle, playing the part of a teacher taking an unruly party of pupils on a daytrip to Salisbury Cathedral. She starred in the BBC sitcom, After You've Gone, alongside Nicholas Lyndhurst and in the ITV1 drama Kingdom, with Stephen Fry. Her part in After You've Gone has, whilst being critically acclaimed, been described as "criminally squandered". In 2013 she guest starred in the hit BBC series Doctor Who where she played the villainous Miss Kiszlet in the series opener The Bells of Saint John
In 2005, she received very positive reviews for her US stage debut in Unsuspecting Susan. In 2009, Imrie appeared in Plague Over England on the West End, a play about John Gielgud, and received positive reviews for her performance Charles Spencer of The Daily Telegraph calling her performance "delicious" and "touchingly sympathetic". In the same year, she appeared in the world premiere of Robin Soans' Mixed Up North, directed by Max Stafford-Clark. In 2010, she appeared alongside Robin Soans in a production of Sheridan's The Rivals. She has appeared with Martin Clunes twice, first in the 2002 John George Haigh biopic A Is For Acid and later in the successful ITV series Doc Martin.