The R&A's 2,400 members around the world have voted overwhelmingly to allow women to join the 'Home of Golf', ending a policy that has been a source of dismay and controversy.
Some 85% of the three-quarters who took part in the ballot were in favour of the change, which club secretary Peter Dawson said would come into "immediate effect".
"I can confirm that The Royal and Ancient Golf Club of St Andrews is now a mixed membership club," he said.
The R&A has been under increasing pressure to admit women
Mr Dawson said the membership had also taken steps to "fast-track a significant initial number of women to become members in the coming months".
He added: "The R&A has served the sport of golf well for 260 years and I am confident that the club will continue to do so in future with the support of all its members, both women and men."
Helen Grant, Britain's minister for sport, said: "I hope we will now see other golf clubs that still have outdated same-sex policies follow suit.
"With golf in the next Olympics there is a huge opportunity for the sport to grow and this sends out the right inclusive message that golf is for everyone."
The decision to poll members was taken after it became clear to Mr Dawson and other influential figures that remaining an all-male bastion was not an option given the club's central role as one of golf's governing bodies.
The R&A is far more than a golf club, setting the rules of the game as it is played by men and women around the world, with the exception of the United States and Mexico.
With that responsibility, the prohibition on women has long seemed anachronistic at best, plain discriminatory at worst, and increasingly untenable given its wider responsibilities.
The R&A separated its commercial and governance function from the private members club at St Andrews 10 years ago, but there is minimal female representation on the committees that effectively govern the game.
That will now change, but only after commercial and political pressure made the status quo untenable.
Two years ago the Augusta National Golf Club, hosts of The Masters, agreed to admit women, making former US Secretary of State Condaleeza Rice the first woman allowed to wear the famous green jacket reserved for members.
Attention will now turn to the three remaining all-male clubs on the Open Championship rota, Muirfield, Royal St George's in Kent, and Troon, with the hope that they will follow suit.
Muirfield and St George's have both begun reviews of their membership policy with a view to change. Troon has said it has no such plans, pointing to the women-only Troon Ladies Club that has access to the course.