The former Wales and British and Irish Lions five-eighth died peacefully in hospital, his family announced on Sunday (Monday AEDT).
John, nicknamed 'The King' by New Zealand journalists after he inspired the Lions' famous 1971 Test series victory in the den of the All Blacks, won 25 Wales caps between 1966 and 1972.
He also played in five Lions Tests on their 1968 and 1971 tours, before retiring from rugby at the age of 27.
Truly one of the greatest. — British & Irish Lions (@lionsofficial) We are hugely saddened that the great Barry John has passed away at the age of 79.Barry inspired so many and will forever be remembered for how much he gave to the sport. All our thoughts are with his family and friends.Rest in Peace. pic.twitter.com/wyI9ZL4FVuFebruary 4, 2024
A statement released by John's family read: "Barry John died peacefully today at the University Hospital of Wales surrounded by his loving wife and four children.
"He was a loving dad to his 11 grandchildren and much-loved brother."
John played his club rugby for Llanelli and then Cardiff, where he struck up a matchless half-back partnership with Gareth Edwards that went on to flourish for both Wales and the Lions.
We are deeply saddened that the great Barry John has passed away at the age of 79.— Guinness Men's Six Nations (@SixNationsRugby) All our thoughts are with his family and friends at this difficult time. Rest in Peace ❤️ pic.twitter.com/47RXtKLTeEFebruary 4, 2024
John was partnered by Edwards in 23 of his Wales international appearances, plus all five Lions Tests - one against South Africa and four against New Zealand.
The immense blow to Welsh rugby came just four weeks after another star of their golden era of the 1970s, fullback JPR Williams, also died.
John was arguably rugby union's first superstar and a mercurial player whose wizardry gained comparisons with footballing genius George Best.
He was rugby royalty in anyone's language. A miner's son from Carmarthenshire, his international career might have lasted only six years before he announced his shock retirement, citing pressures of fame and expectation as he stepped down before his 28th birthday, but it was glorious while it lasted.
An imperious No.10, he had a seemingly effortless ability to beat defenders in a manner that often defied logic and gained him worldwide admiration.
Edwards once wrote of his halfback partner: "He had this marvellous easiness in the mind, reducing problems to their simplest form, backing his own talent all the time.
"One success on the field bred another and soon he gave off a cool superiority which spread to others in the side."
Born in the village of Cefneithin to William and Vimy John, he was one of six children. All three of his brothers - Delville, Alan and Clive - played rugby.
John began his career at Llanelli, making a first team debut against Moseley two days before his 19th birthday in 1964. Two years later, he was capped by Wales and in 1967 he moved to Cardiff and played alongside Edwards.
John scored 30 of the Lions' 48 points across four Tests in New Zealand in 1971, and the flickering black-and-white TV pictures showcased him in all his glory as a player.
Then, he shocked rugby by calling it a day at a time when he was still the sport's biggest name.
"I was the first rugby pop star, superstar, call it whatever you want," John once recalled.
"I didn't want to retire, but it was the circumstances. People didn't understand how you had to go to work, how you had to be fit for international-level rugby.
"I was getting lethargic, tired. You can't be like that on the international stage, especially at number 10."
His legacy was one that most players could only dream of. Wales won three Five Nations titles, a grand slam and two triple crowns during his reign.