[4] She joined the Cambridge Footlights and wrote and performed in the comic revue Far Too Happy, which toured Britain for three months and gained the troupe's first Perrier Award nomination in 20 years.

[7] Winkleman's credits include recurring roles in series including Big Suze in Peep Show,[8] numerous roles in Harry & Paul,[9] Joely in White Teeth,[10] Fiona in The Trial of Tony Blair,[11] Abby in Plus One,[12] Katerina in Red Dwarf: Back to Earth,[13] Donna in Lead Balloon,[14] Prudence in Keen Eddie, Elle Kensington in Chasing Alice, Regan Peverill in the pilot episode of Lewis, Angela Warren in Agatha Christie's Poirot (in the episode "Five Little Pigs"), Princess Eleanor in The Palace,[15] Ghislaine in Robin Hood,[16] Alice Shadwell in Dalziel and Pascoe, Ann Hamilton in Death in Paradise,[17] Jill in TV Land's Hot in Cleveland, Sharon Kirby in CSI Miami[18] and Dorothy Gibson in Titanic.

[22] Winkleman's roles while at Cambridge University included the Bride in García Lorca's Blood Wedding,[23] which toured the amphitheatres of Greece, Elizabeth in Six Degrees of Separation,[23] which played at the Edinburgh Festival, Abigail in Arthur Miller's The Crucible,[18] Dockdaisy in Bertolt Brecht's The Resistible Rise of Arturo Ui,[23] Kate in Alan Ayckbourn's Confusions,[23] Madame de Merteuil in Christopher Hampton's Les Liaisons Dangereuses[23] and Fraulein Kost in Kander and Ebb's Cabaret all at the ADC.

[23] In 2012 she played Helena in Eric Idle's musical What About Dick at the Orpheum Theatre in downtown Los Angeles, alongside Eddie Izzard, Russell Brand and Billy Connolly.

[23] Winkleman played the comic role of Debbie Levine in Pathe's romantic comedy Suzie Gold and the older Susan Pevensie in the Disney film The Chronicles of Narnia: The Lion, the Witch and the Wardrobe.

[18] Other film roles include the leads in the shorts Seared, Love Letters, and The Lost Domain, a cinematic take on Alain-Fournier's Le Grand Meaulnes, and Post, directed by Debs Gardner-Paterson.

Wodehouse's Uncle Fred in the Springtime with Alfred Molina and Rufus Sewell, Gloria in Bernard Shaw's You Never Can Tell, and Zoe in Alan Ayckbourn's Henceforward, alongside Jared Harris, all for Radio 4.