Differentiation of genera of the modern (Late Miocene to Recent) South American rodent family Ctenomyidae would have been linked to the acquisition of disparate adaptations to digging and life underground. In accordance with this hypothesis, the delimitation of lineages and genera in the ctenomyid fossil record is evaluated here following an adaptation-rooted criterion that involves both an assessment of the monophyly and of the adaptive profiles of recognized clades. The application of such a criterion, including morphofunctional information, delimited four cohesive lineages among crown ctenomyids (i.e. euhypsodont species of the Late Miocene to Recent): Eucelophorus (Early Pliocene–Middle Pleistocene), Xenodontomys-Actenomys (Late Miocene–Pliocene), Praectenomys (Pliocene) and Ctenomys (including Paractenomys; Pliocene–Recent); in addition, the results supported the status of Xenodontomys as a paraphyletic ancestor of Actenomys. The cladogenesis that gave rise to the crown group would have occurred immediately after the acquisition of euhypsodonty in a Xenodontomys simpsoni-like ancestor during the Late Miocene. This putative ancestor would have had fossorial habits and moderate digging specializations, an adaptive profile maintained in Xenodontomys-Actenomys. Eucelophorus and Ctenomys would have independently evolved subterranean habits at least since the Pliocene. Although the earliest history of the only living representative, Ctenomys, is known only fragmentarily, remains from Esquina Blanca (Uquía Formation), in north-western Argentina, suggest a minimum age of around 3.5 Ma (Early–Late Pliocene) for the differentiation of the genus. This date agrees with recent molecular estimates.