Ainslie said he will remain as CEO and majority owner of his British SailGP team as well as principal and skipper for INEOS Britannia, his British challenger for the 37th America's Cup, which will take place in Barcelona later this year.
Scott will take over at the next event in SailGP's fourth season, on January 13-14 in Abu Dhabi, with Ainslie focusing on the team's performance and on promoting sailing's next generation.
"It's time to give younger sailors the opportunity," said Ainslie, who in 2022 set up the Athena Pathway Programme, which aims to fast-track the development of youth and female sailors and bring more diversity into sailing.
The decision to let go of the F50 wheel was probably the toughest of his sporting career, Ainslie said in a statement.
"As the CEO of both Emirates GBR and the INEOS Britannia America's Cup Team, and most importantly a husband and father, at some point you've got to realise that you can't do everything," he said.
"We've got a huge talent in Giles Scott, he's one of the best in the sport and he will suit this style of racing perfectly," he said, adding he was going to be part of SailGP for "many years to come".
Scott joins as 'driver' alongside strategist Hannah Mills, who is the most successful female Olympic sailor and is working to become the first woman to helm a SailGP team.
"I've got to step up to the mark and do the best job I can to fill those big old boots that Ben's left behind," said Scott of his one-time rival and long-term team mate Ainslie.
The British team are attempting to win the $1 million prize SailGP series, which has been dominated by Australia, for the first time. They lie in fourth position in the 13-event series, which is due to culminate in San Francisco in July.