Cambrai's famous bishop Pierre d'Ailly took an active part in the Council of Constance (1414-1418), and Dufay's presence in his retinue could explain several points: his absence from Cambrai from November 1414, his early exposure to English music, and his contacts with the Malatesta family. After a brief tenure as subdeacon in Cambrai's St.-Géry, Dufay took up service with the Malatesta in Pesaro/Rimini. Two lavish wedding pieces, another motet, and a number of chansons date from this service, probably from 1420-1424. The health of his mother caused Dufay to return North, likely settling briefly in Laon, but the composer left for Italy again in 1426, bidding farewell to the fine wines of his homeland in the autobiographical Adieu ces bons vins.
Dufay stayed for some months in Bologna in the retinue of Cardinal Louis Aleman, possibly beginning his law degree there, but by December 1428 he had assumed a lucrative post in the Papal Chapel. Under Pope Martin V, the Chapel singers enjoyed a strong salary as well as the opportunity to hold several absentee benefice incomes; the musicians' fortunes improved further under the patronage of his successor, Eugenius IV (for whom Dufay wrote three more motets). However, Roman political turmoil helped push Dufay into the waiting arms of the Ducal Court of Savoy in 1433. As choirmaster there, his compositional life flourished, yielding a large cycle of hymn settings and many mature songs. A 1435 promotion to first singer (and choirmaster) lured him back to the Papal Chapel, now resident in Medicean Florence; among other pieces, Dufay gave the City of the Lily Nuper rosarum flores for the completion of Ghiberti's dome and the consecration of her Cathedral.
Dufay returned to a canonicate at Cambrai Cathedral by December 1439, where he remained for most of the remainder of his life. Only a trip to Italy in 1450, possibly to contribute the St. Anthony Mass for the dedication of Donatello's altar in Padua, and a final period of Savoyard service from 1452 to 1458, broke this semi-retirement. He took on a number of administrative tasks, such as ambassador to the Court of Burgundy (with which he apparently maintained a lifelong relationship), and musically led the petit vicaires as well as supervising the recopying of the Cathedral's chantbooks. He also composed several late cantus firmus masses, a lost requiem, and a plainchant Marian Office. At his death in 1474, Dufay left a sizable fortune (including cash, jewelry, furniture, and books), as well as musical provisions for his own memorial services. He also left an outstanding musical reputation and an exceptionally long shadow upon generations of composers to come.