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After moving to London, her first novel, Oranges Are Not the Only Fruit, won the 1985 Whitbread Prize for a First Novel, and was adapted for television by Winterson in 1990. This in turn won the BAFTA Award for Best Drama. She won the 1987 John Llewellyn Rhys Prize for The Passion, a novel set in Napoleonic Europe.
Winterson's subsequent novels explore the boundaries of physicality and the imagination, gender polarities, and sexual identities, and have won several literary awards. Her stage adaptation of The PowerBook in 2002 opened at the Royal National Theatre, London. She also bought a derelict terraced house in Spitalfields, east London, which she refurbished into a flat as a pied-a-terre and a ground-floor shop, Verde's, to sell organic food.
Winterson was made an officer of Order of the British Empire (OBE) at the 2006 New Year Honours "For services to literature".
In 2009, she donated the short story Dog Days to Oxfam's Ox-Tales project comprising four collections of UK stories written by 38 authors. Winterson's story was published in the Fire collection. She also supported the relaunch of the Bush Theatre in London's Shepherd's Bush. She wrote and performed work for the Sixty Six project, based on a chapter of the King James Bible, along with other novelists and poets including Paul Muldoon, Carol Ann Duffy, Anne Michaels and Catherine Tate.
In 2012, she succeeded Colm Tóibín as Professor of Creative Writing at the University of Manchester