Northampton North MP, Michael Ellis, has also been given an extra role as Cabinet Office minister alongside his existing role as Paymaster General.
Mr Heaton-Harris, who was only moved to the Foreign Office a few weeks ago, was one of three names in the hat to be handed the key post.
The Brexit hardliner and Johnson loyalist — reported to have been a central figure in the so-called 'Operation Save Big Dog' — will be tasked with the job of rebuilding trust in the PM among Conservative backbenchers.
South Northamptonshire MP Dame Andrea Leadsom hailed his appointment on Twitter, posting: "Such a good choice! Chris will provide the fresh impetus the government needs."
Corby's Tom Pursglove said: "A terrific appointment and richly deserved — a great Northamptonshire colleague!"
Mr Heaton-Harris, 54, who has been Daventry's MP since the Tories reclaimed power in 2010, will hold the official title of Parliamentary Secretary to the Treasury.
He was previously Minister of State at the Foreign, Commonwealth & Development Office from December 19, 2021; and transport minister for two years before that.
The chief whip is responsible for administering the system that ensures party members attend and vote in Parliament as the leadership desires.
The previous chief whip, Mark Spencer, has been moved to Leader of the House of Commons where he replaces Jacob Rees-Mogg, a statement from No 10 said.
Mr Rees-Mogg will be the minister responsible for 'Brexit opportunities' in the first move confirmed as part of Mr Johnson’s widely anticipated mini-reshuffle.
The shake-up of the ministerial team follows the appointment of Stephen Barclay as the Prime Minister’s chief of staff and comes as Mr Johnson seeks to relaunch his administration following the partygate row.
Mr Ellis has been a regular at the Commons dispatch box in recent weeks tasked with fending off opposition calls for answers from the Prime Minister over Partygate.