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Ben Elliot has resigned as Conservative co-chairman following Liz Truss's election as party leader.
Mr Elliot oversaw a huge increase in donations to the party from wealthy individuals after his friend Boris Johnson gave him the role in 2019.
But he has also faced questions over his business interests and fundraising methods.
Last week, Labour urged Ms Truss and her then leadership rival Rishi Sunak to sack Mr Elliot if they became PM.
Announcing his resignation, Mr Elliot said it had been a "huge honour and privilege" to serve the Conservative Party.
"I would like to thank Boris Johnson for appointing me, and wish Liz Truss every success in leading our great country, particularly given the challenges of the winter ahead," he added.
A friend of Mr Elliot told the Daily Mail he wanted to give Ms Truss, who was earlier announced the winner of the contest to succeed Mr Johnson as Tory leader and PM, the freedom to appoint her own party chair.
The nephew of Camilla, Duchess of Cornwall, Mr Elliot was educated at Eton and is known for being well-connected.
His company, Quintessentially, helps provide its wealthy clients with all the trappings of a luxury lifestyle - from yacht hire and holiday booking to private concerts with pop stars.
But last year, he was warned by a lobbying regulator to keep his private business interests and public role as Tory co-chairman separate.
It followed reports suggesting Quintessentially had arranged access to top politicians for clients.
Last week, Labour urged the next Conservative leader to sack Mr Elliot from his role.
In a letter to both Liz Truss and Rishi Sunak, seen by PoliticsHome, Labour Party chair Anneliese Dodds raised concerns about the Tory donors' club he reportedly established.
Ms Dodds called on the party to reveal the names of those involved in the group after repeated refusals in recent years.
Commenting on Mr Elliot's departure, Conservative Party chief executive Darren Mott said: "The whole Conservative Party wants to thank Ben Elliot for his tireless service over the past three years.
"Without his incredible efforts, the 2019 landslide would not have been possible. We wish him all the best in his future endeavours."