He was one of the few men to have served as councillor to Kings Edward IV, Richard III and Henry VII and was trusted by all of them.

After Edward IV's accession, he became a member of the privy council and was created Baron Dynham in 1467, although no grant of lands accompanied the title, as was usual.

In that capacity, he recaptured Hammes Castle, which had defected to Henry VII, but was criticised for allowing the garrison to depart.

[7] While the Zouche connection had been useful, Dynham acquired a new patron in Lord Willoughby de Broke, his second wife's father, who was Steward of the Royal Household.

Certainly, Dynham flourished under Henry; he was made a Knight of the Garter,[2] and was Lord Treasurer from 1486 until his death: he took his duties at the Exchequer very seriously and spent most of his time at Lambeth for convenience.

[citation needed] John Dynham married twice: He also had an illegitimate son, Thomas Dynham (died 1519), who was granted lands in Eythrope, Buckinghamshire, [2] and who married Joan Ormond, eldest daughter of John Ormond (died 1503) and Joan Chaworth.

[13] As he died without surviving children, his estates, which included Nutwell, Kingskerswell and Hartland, Devon, along with Souldern, Oxfordshire (inherited from Arches family), descended to the heirs of his four surviving sisters (a fifth sister, Edith, appears to have predeceased him, leaving no issue):[14] A wool and silk tapestry manufactured in the Southern Netherlands exists in The Cloisters Collection in the Cloisters Collection of the Metropolitan Museum of Art in New York that illustrates Lord Dynham's armorial bearings and heraldic badges set against a millefleurs backdrop.

[27][30][31][32] Two years later, in 1488, King Edward permitted Jean Pasquier to import into the country, duty free, altar cloths and tapestries, and according to Bonnie (1962) Dinham may have ordered one for himself at the same time.

[29][27] The central image of the tapestry is an escutcheon in the shape of a jousting tournament targe surrounded by a blue Garter.

[27][35][28] The family Badge of the Dynhams was the head of a hart, again in allusion to Hartland Abbey,[36] Lord Dynham's personal badge comprises: "a topcastle of a warship, broken at the mast, with five javelins resting inside the structure against the railing, and flying a swallow-tailed pennant with red and white streamers and a cross of Saint George next to the staff" and is repeated eleven times throughout the millefleurs ground, which was originally dark green, but appears blue today.