In February 2022, he was appointed to the Cabinet as Chief Whip of the House of Commons and Parliamentary Secretary to the Treasury, and was sworn in as a privy counsellor.

Heaton-Harris worked for the family business at New Covent Garden Market, before taking over from his father running What4 Ltd for eleven years.

[12] At the 1997 general election Heaton-Harris unsuccessfully contested the constituency of Leicester South, finishing second with 23.7% of the vote behind the incumbent Labour MP Jim Marshall[13][14] He again unsuccessfully contested the seat in the 2004 Leicester South by-election, finishing third with 19.7% of the vote behind the Liberal Democrat Parmjit Singh Gill and Labour's Peter Soulsby.

[28] In February 2022, he was appointed by Johnson as Chief Whip of the Conservative Party and was subsequently sworn into the Privy Council of the United Kingdom.

[31] Heaton-Harris accepted tickets for himself and his family to attend four events at the London 2012 Olympics relating to swimming, diving, gymnastics, and the closing ceremony, as a gift from Coca-Cola.

[12] Heaton-Harris was one of several MPs, including Labour's shadow whip Mark Tami, who received tickets worth £1,961 to the England v Germany game at the 2020 UEFA European Football Championship from Power Leisure Bookmakers.

[32] In November 2012, covert video footage of Heaton-Harris discussing the role of James Delingpole in the Corby by-election were published on the website of The Guardian.

The recording, made by Greenpeace, appeared to show the MP's support for Delingpole's independent, anti-windfarm candidacy, at a time when Heaton-Harris was engaged by the Conservatives to run the unsuccessful campaign of their own candidate, Christine Emmett.

Heaton-Harris indicated that this was linked to a plan by core members of the Conservative Party to emasculate the Climate Change Act by making its commitments advisory rather than mandatory.

[33] After Heaton-Harris apologised for the impression he gave in the video, Home Secretary Theresa May said he was guilty only of silly bragging, while Labour's Michael Dugher MP urged Prime Minister David Cameron to show leadership and punish him.

[37] In addition, the letter attracted criticism from both pro-Remain and pro-Leave academics at Cambridge and London's Queen Mary universities, and a rebuke from Downing Street.

[38][39][40] Responding the next day to the widespread criticism from both politicians and academics, universities minister Jo Johnson suggested that Heaton-Harris might have been researching a possible book on "the evolution of attitudes" to Europe, rather than acting in his role as a government minister, and "probably didn't appreciate the degree to which (the letter) would be misinterpreted",[41] although there was no mention of any research for a possible book in the original letter.

[43][44][45] At the same time he sat on the wide-ranging powers of the European Scrutiny Committee,[6][5] set up to assess the legal and/or political importance of draft EU legislation.

[46] Documents from the House of Commons catering department released via Freedom of Information to openDemocracy, show Heaton-Harris hosted an ERG breakfast meeting in October 2017, despite taking over as a government whip in July 2016.