The spelling of Ockeghem's name comes from a supposed autograph of his which survived as late as 1885, and was reproduced by Eugène Giraudet, a Historian in Tours; the document has since been lost. In 15th-century sources, the spelling "Okeghem" predominates.

In 1993, documents dating from 1607 were found stating that "Jan Hocquegam" was a native of Saint-Ghislain in the County of Hainaut, which was confirmed by references in 16th century documents. This suggests that, though he first appears in records in Flanders, he was a native speaker of Picard. Previously, most biographies surmised that he was born in East Flanders, either in the town after which he was named (present-day Okegem, from which his ancestors must have come) or in the neighboring town of Dendermonde (French: Termonde), where the surname Ockeghem occurred in the 14th and 15th century. Occasionally, Bavay, now in the Nord department in France, was suggested as his birthplace as well.

A strong influence on Josquin des Prez and the subsequent generation of Netherlanders, Ockeghem was famous throughout Europe for his expressive music, though he was equally renowned for his technical prowess. Two of the most famous contrapuntal achievements of the 15th century include his Missa prolationum, which consists entirely of mensuration canons, and the Missa cuiusvis toni, designed to be performed in any of the different modes, but even these technique-oriented pieces demonstrate his uniquely expressive use of vocal ranges and tonal language. Ockeghem's use of wide-ranging and rhythmically active bass lines sets him apart from many of the other composers in the Netherlandish Schools.