John was the bastard son of Sir John Golafre Senior (d. 1379) of Fyfield Manor in Berkshire, by his mistress, Janet Pulham. His parents' relationship must have lasted a number of years, since there was also a daughter, Alice, who became the Prioress of Burnham Priory in Buckinghamshire. However, despite Sir John Senior having no other offspring by his two marriages, his legal heir was his nephew, also John, so young Golafre stood little chance of inheriting his father's widespread estates the Southern Midlands and Northern Wessex.

John therefore looked to a career in Royal service to make his way in life and he was probably helped in this by his step-mother's brother, the Master of the King's Horse, Sir Bernard Brocas. He almost certainly started out as a soldier in the King's army, serving in France. By 1384, however, John had obtained a placement in the household of King Richard II and was made an Esquire of the King's Chamber. In the same year, he acquired land forfeited by the imprisoned London politician, John Northampton. The following year, John fought bravely with King Richard's forces during their invasion of Scotland and, there, he was knighted.

This clearly brought him to the fore in the King's favour and, in 1387, he was sent on Royal diplomatic missions, as well as being appointed to the trusted position of Keeper of the King's Jewels and Plate.  Sir John visited France to organise peace negotiations with King Charles VI where he was to act on behalf of King Richard. However, this brought him into conflict with the Duke of Gloucester and the other English nobles opposed to the ending of War. In the December, orders were issued for his arrest and he was obliged to stay abroad for some time. The eventual French truce agreed in 1389 meant there were now limited opportunities for armed campaigning, but he kept his hand in on the tournament circuit. In March/April 1390, he is recorded amongst the English knights at the famous St. Inglevert tournament near Calais, where Jean Boucicault and his friends challenged all comers, and he rode against Sir Reginald de Roye. They smashed each others helmets in the first round, but neither were unhelmed and their lances also survived serious damage. In the second, their horses refused to charge, but, in the third, they struck shields and broke their lances. There were no strikes in the last round and the two retired from the tilting yard. 

Back in England, Sir John managed to acquire positions controlling more static military installations. He was appointed Constable of Wallingford Castle in 1389, followed by Flint Castle in North Wales and Nottingham Castle in the Midlands by 1392. In that year, he was also made responsible for ensuring that all yeomen in the King's household had bows and regular archery practice, so they could act as Richard's personal bodyguard. Sir John was also made Captain of Cherbourg and continued with his diplomatic duties abroad. In 1394, he was sent to Poland to gather support for the Anglo-French crusade against the Turks. He was away from home for a whole year but, while the exact results of his mission are unknown, few Poles appear to have joined the cause. The following year, he accompanied the King's forces on their two expeditions to Ireland.

At various times, Sir John acquired an interest in additional lands and therefore revenue: life-ownership of Shotwick Manor in the Wirral and co-custody of the estates of the Earl of Pembroke after his death in 1389. Towards the end of his life he also gained control of Becklay and the Forest of Wychwood in Oxfordshire. However his income probably amounted to less than £400 a year, not a great amount for a man of his standing. He may have hoped that a good marriage would help. However, when he married the Mohun co-heiress, Philippa, Lady FitzWalter, her mother  sold off most of her daughters' inheritance before she could claim it. Sir John eventually died at Wallingford Castle on 18th November 1396, aged only about forty-five. He had asked to be buried in the family mausoleum at the Greyfriars' Church in Oxford but, on his deathbed, King Richard persuaded him that Westminster Abbey was a more fitting site. He was therefore laid to rest under a fine memorial brass adjoining both the shrine of St. Edward and the plot allocated to the King. He left no children but, in his will, he remembered a number of family members, as well leaving the King his best horse, his white-hart badge, gold cup, gold chain and sapphire encrusted stone.