Announced at a pop-up bar in Harrogate on Thursday during the UCI Road World Championships, UCI president David Lappartient said the "exciting" partnership would help make cycling the sport for the 21st century.
Unlike other electronic sports, the esports cycling world championships will involve intense physical activity with riders racing on static bikes linked to the Zwift platform.
Zwift was launched in 2014 and allows cyclists to train on some of the sport's classic routes from the comfort of home using their own bike on a turbo-trainer linked to a screen.
So-called Zwifters have already ridden more than two million 'virtual' miles on UCI Road World Championship courses, including the ongoing one in Yorkshire.
Britain held the inaugural national esports cycling championships last year.
"We have been looking at the emergence of esports for some time with Zwift," Lappartient told a news conference.
"We need to remain open to technical innovations and change, and to remain relevant to all audiences. Zwift is a platform that is enjoyed by people of all ages and abilities.
"Together we have an opportunity to support a fitter youth, through the creation of a new sustainable sport. We want to make cycling the sport of the 21st Century."
The partnership will see both implement a new UCI rule book for cycling esports in the coming year.
It is yet to be decided on the venue or the format for the championships, although wherever it is riders will be at least spared the torrential rain that has blighted the actual championships around Yorkshire this week.
Craig Edmondson, CEO of Zwift Esports, said the championships would see both sexes competing over the same distances and sharing equal prize money.
"We want to deliver fair competition and grow the sport of cycling and get more people active, more often," Edmondson said.
"I'm excited to be able to build a sport, or a discipline, from scratch. And we will do that with parity for men and women. It's a new chapter in the sport's history.
"We will set the standard for fair play and equality."
In April this year bike maker Canyon launched the first ever professional e-racing team: Canyon ZCC.
"Racing on Zwift is in its infancy, but compared to the cost of running a traditional cycling team, starting Canyon ZCC was a no-brainer of an opportunity," team manager Rhys Howell said.
The Cycling Central podcast is sponsored by Zwift.