His time was 3 minutes, 59.4 seconds and the crowd erupted into rapturous cheers as soon as the announcer read out "three", confirming he'd broken the four-minute mile.
Swedish runner Gundar Haegg's mile time of 4:01.4 had stood for nine years, but in 1954 Bannister, Australian rival John Landy and others were threatening to break it.
The two men competed at the Commonwealth Games in Canada later in 1954 in a race billed as the "Miracle Mile".
By then Bannister was having trouble walking, let alone running, after revealing he was suffering from Parkinson's disease.
"He banked his treasure in the hearts of his friends", they added, in a statement published by the Press Association news agency.
Roger Bannister about to cross the tape at the end of his record-breaking mile run at Iffley Road, Oxford.
Prime Minister Theresa May paid respects to the late athlete on social media "Sir Roger Bannister was a great British sporting icon whose achievements were an inspiration to us all".
But Bannister's achievement has continued to inspire athletics enthusiasts, with the shoes he wore to break the four-minute barrier selling for a record.
"He was an inspiration to those like me who sought to combine university with worldwide sport".
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He entered the 1952 Olympic Games in Helsinki as the United Kingdom record-holder in the mile, finishing a disappointing fourth in the 1,500-meter run.
"None of my athletics was the greatest achievement", he said. It was the first time two men had run under 4 minutes in the same race.
The condition progressively damages part of the brain over time and is one Bannister was familiar with, even before he was first diagnosed a few years ago, from his lengthy career as neurologist.
Steve Ford, chief executive of Parkinson's United Kingdom said: "We're very saddened to hear of the death of Sir Roger Bannister".
He also became the first chairman of the body now known as Sport England (formerly the Sports Council) and was knighted for his services in 1975.
TeamGB: "We are incredibly saddened by the death of Sir Roger Bannister, aged 88".
"There is not a single athlete of my generation who was not inspired by Roger and his achievements both on and off the track", Coe tweeted.
Bannister married Moyra Jacobsson, an artist, in 1955.
Bannister returned to Oxford in 1985 to become Master of Pembroke College, a position he held until 1993.