Ms Wheatcroft's appointment follows the departure of former editor Sarah Sands, who leaves after 11 years working across the Daily Telegraph and Sunday Telegraph.
Commenting on her appointment, Ms Wheatcroft said: "The Sunday Telegraph is a great newspaper and I am very excited by the challenge of taking over the leadership at this very opportune moment of a paper that stands for so many of the things I believe in."
Before the Times, she worked on the financial sections of the Mail on Sunday and the Daily Mail, and was also editor of Retail Week.
She was awarded London Press Club Business Journalist of the Year in 2003.
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