The internal carotid artery (ICA) is one of the major vessels in the cranial circulation. Characters concerning the ICA, such as its course in the auditory region, have been employed frequently in phylogenetic analyses of mammals, including extinct taxa. In lagomorphs, however, our knowledge on vascular features of the auditory region has been based predominantly on living species, mostly on the European rabbit. We present the first survey on 11 out of 12 extant genera and key fossil taxa such as stem lagomorphs and early crown representatives (ArchaeolagusandProlagus). The ICA pattern shows a modified transpromontorial course in stem taxa (Litolagus,MegalagusandPalaeolagus) andArchaeolagus, which we propose as the ancestral character state for Lagomorpha, similar to that for the earliest rodents, plesiadapids and scandentians. The ICA pattern in leporids is perbullar, but shows structural similarities to stem taxa, whereas the extrabullar ICA course inOchotonais apparently a highly derived condition.Prolagusshows a mixed character state between leporids andOchotonain its ICA route. The persistence of the transpromontorial ICA course and similarities in the carotid canal structure among stem taxa and crown leporids support morphological conservatism in Lagomorpha, in contrast to their sister clade Rodentia.This article is part of the theme issue ‘The mammalian skull: development, structure and function’.