Abstract Aim Species or higher taxa that are obviously dispersal‐limited, but which occupy large geographical distributions, represent a biogeographical paradox. Dispersal must have happened, likely under special and infrequent environmental conditions, but details have been lost to history. The overarching goal of our research is to understand the details of a ‘common vicariance, rare dispersal’ biogeographical history in a widespread but habitat‐specialized harvestman species ( Sabacon cavicolens ) with a southern Appalachian centre of distribution. Location Eastern North America, southern Appalachians. Methods We assessed cryptic speciation using mitochondrial and nuclear gene DNA sequence data, testing alternative delimitation hypotheses using multispecies coalescent analyses. We also tested whether riverine barriers are associated with mitochondrial genealogical structuring, focusing on multiple rivers in the southern Blue Ridge physiographical province. Finally, we conducted population genetic analyses to assess female‐based range expansion out of the southern Blue Ridge. Results Genetic analyses suggest a large number of species‐level lineages within S. cavicolens , although we prefer a more conservative three‐species hypothesis. These putative species are geographically cohesive and allopatric (Ozarks, Cumberland Plateau, southern Blue Ridge), with the Blue Ridge species including multiple divergent mitochondrial haplogroups. Several genealogical breaks in the Blue Ridge species coincide with riverine barriers, separating mostly allopatric mitochondrial lineages. Contrasting with evidence for constrained gene flow and vicariance, two Blue Ridge haplogroups reveal extensive range expansion both northwards and westwards, resulting in the widespread distribution of closely related haplotypes, and occasional sympatry of dispersive haplotypes. Main Conclusions Hidden beneath the apparently widespread distribution of a single species is a history of old vicariance separating geographically disjunct cryptic ...