Recent advances in genomics and palaeontology have begun to unravel the complex evolutionary history of the gray wolf, Canis lupus. Still, much of their phenotypic variation across time and space remains to be documented. We examined the limb morphology of the fossil and modern North American gray wolves from the late Quaternary (< ca.70 ka) to better understand their postcranial diversity through time. We found that the late-Pleistocene gray wolves were characterised by short-leggedness on both sides of the Cordilleran-Laurentide ice sheets, and that this trait survived well into the Holocene despite the collapse of Pleistocene megafauna and disappearance of the “Beringian wolf” from Alaska. In contrast, extant populations in the Midwestern United States and north-western North America are distinguished by their elongate limbs with long distal segments, which appear to have evolved during the Holocene possibly in response to a new level or type of prey depletion. One of the consequences of recent extirpation of the Plains (C. l. nubilus) and Mexican wolves (C. l. baileyi) from much of the United States is an unprecedented loss of postcranial diversity through removal of short-legged forms. Conservation of these wolves is thus critical to restoration of the ecophenotypic diversity and evolutionary potential of gray wolves in North America.