Dunstable disappears from the historical record until 1427, when it is established that he was then in France in the service of Henry V's younger brother John of Lancaster, Duke of Bedford. Dunstable is also shown to be in the retinue of the notorious dowager Queen, Joan of Navarre, from 1428. The historical record relating to Dunstable's service to the Plantagenets is unclear, but this may mean that Dunstable traveled quite frequently between England and France, in service of both courts. During his travels abroad Dunstable may have become acquainted with his greatest admirers, the Franco-Flemish composers Guilliaume Dufay and Gilles Binchois. Fifteenth century treatises acknowledge the impact made by English music on French musicians during this period. This reflects the concurrent political situation as well, as much of the territory of France, including Paris itself, lay in English hands from 1420 to 1450, the final phase of the Hundred Years War. Dunstable benefited directly from this situation when the Duke of Bedford died in 1435, as Bedford awarded to Dunstable generous land grants in Normandy. Queen Joan remembered him a handsome annuity at her death in 1437. Dunstable was also an astronomer of considerable acclaim in his day, and astronomical charts believed to be in his own hand yet survive. However, all of his music is only known in copies made by other scribes. Most of Dunstable's music is preserved in sources located in Italy and Germany, rather than England, where just a scant remainder of contemporary examples remains.
Only a tiny fraction of Dunstable's work is of the secular variety, and of these the most widely circulated piece, O Rosa bella, is now known to be the work of Dunstable's younger contemporary John Bedyngham. Although Dunstable's musical output is primarily sacred, there is no evidence to suggest that he held any post as a cleric. When Dunstable died in 1453, he was both wealthy and famous, and his reputation as a composer survived well into the first part of the sixteenth century. Another presumed associate of Dunstable's, John Wheathampstead, abbot of Saint Albans, composed two epitaphs to Dunstable's memory, one of which reads "with (Dunstable) as judge, Urania learned how to unfold the secrets of Heaven. This man was your glory, O Music; who had dispersed your sweet art through the world. The 'star' transmigrates to the stars; may the citizens of Heaven receive him as one of their own."