John was the only son of Thomas Foxley, the Constable of Windsor Castle, and his wife, Katherine, the daughter and co-heiress of Sir John Ifield of Apuldrefield in Cudham in Kent and Swallowfield in Berkshire. He was named after his grandfather, a prominent Baron of the Exchequer, and his childhood would have been spent largely at his father's manor of Bramshill in Northern Hampshire. Although, he would also have resided with his grandmother at Foxley's Manor in Bray when the family wished to be a bit nearer his father, whose work often kept him away at Windsor. As John grew up, he would, no doubt, have spent more and more time at Windsor Castle himself, helping his father and, eventually, becoming a squire.

The following year, the aged Constance Foxley died and Constable Thomas and his family moved back to Bray. Whether John and his young bride went too is unclear. They may have stayed at Bramshill to raise the son and two daughters who quickly joined them in subsequent years. We find little recorded of John Foxley for the next thirty years and we may safely assume that, for a large proportion of the time, he was away in France fighting for Edward III. Like both his father-in-law and brother-in-law, he probably took part in the great English victories at Crecy (1346) and Poitiers (1356). Whilst, during periods of truce, he must have spent his time shuttling between Foxley Manor, where he had permission, long before his father's death, to hold divine service in the chapel, and Bramshill Manor. Indeed, John may well have been employed by his father in some administrative capacity connected with the rebuilding of Windsor Castle, as well as in the transformation of his latter manor house into a grand fortress itself. He certainly became a good friend of the Windsor  architect and subsequent Bishop of Winchester, William of Wykeham.

By the time of his father's death and John's succession to the family estates, in 1360, the latter had obviously come to the attention of the King. At some point, he was knighted and, in 1365, he was made the first Constable of 'Sheppey Island Castle' (otherwise known as Queenborough) for life. The castle was still being built at the time, so presumably the appointment was due to his familiarity with castle building. It may even indicate an earlier involvement with the construction of the 'Round Table' Building at Windsor which, like Queenborough, was circular in plan. Eleven years later, he moved on to be Constable of Southampton Castle too, probably for similar reasons. Like Windsor, the fortress was about to undergo a major rebuilding programme in view of the constant threat of a French invasion. Sir John was also Warden of the King's Manor and Park of Lyndhurst, and of the New Forest, for which he received, from King Edward, a splendid bugle-horn mounted with gold and the Wardenship's insignia, the true mark of a Royal favourite. It was possibly during his sojourns in the south that Sir John entered into a liaison with a penniless girl called Joan Martyn. The two had at least three sons together (the eldest of whom later claimed that his mother was from a younger branch of the Martyns of Athelhammpton in Dorset). Sir John must still have spent much time at home however. For 1376 was also the year in which he was one of nine who were to set the county of Berkshire in array and he did sit in nine parliaments at the end of Edward's reign - seven times for Berkshire and twice for Hampshire. The Royal grant he obtained for a house in Fleet Street (Westminster), must have come in very handy. The date of Lady Foxley's death is unknown, but, not long afterwards, Sir John married his lover, Joan Martyn, and presumably his young illegitimate family moved to Bramshill or Bray.

Sir John died the year after his great patron, King Edward III, in November 1378. By his will, made at Bramshill Castle, he directed his executors - including his first wife's, cousin, Arnold Brocas - to be guided in certain matters by the "ordering and consent" of his friend, Bishop Wykeham, to whom he left a valuable gold ring set with a sapphire. As William, his son by Matilda, had died two years previously, by a peculiar quirk of English law, Sir John was succeeded in his estates - of Foxley (Bray) and East Court (Finchampstead) in Berkshire, Bramshill in Hampshire, Apuldrefield (Cudham) in Kent and Rumboldswyke in Sussex - by his eldest illegitimate son, Thomas, who was designated 'bastard aisné.' His eldest legitimate heir, Katherine, the wife John Warbleton of Sherfield-upon-Loddon (Hampshire) and Warbleton (Sussex),  could not have been best pleased however and there were major land disputes in later generations. Sir John Foxley was buried in the family chapel of All Saints in Bray parish church. In his will, he left very specific instructions for the erection of a fine marble tomb over his body, inlaid with incised brass effigies of himself and his two wives in full armorial outfits. This can still be seen there today, although it has now been removed to the wall of the north aisle.