The current patterns of biodiversity have significantly been affected by glacial-interglacial cycles during the Pleistocene period. True freshwater crabs are considered as poor dispersers and terrestrial barriers restrict gene flow between their local populations. Recent studies, however, suggest that certain environmental conditions, such as periods of heavy rainfall and humidity, can facilitate their between-drainage dispersal and will result in the evolution of homogenous genetic patterns among different drainage systems. Here we tested this hypothesis by comparing populations of the endemic freshwater crab Potamon elbursi Pretzmann, 1962 distributed in two drainage systems, the Caspian Sea and Namak Lake, in northern Iran. Our results based on the genetic analysis of 70 new and 61 previously published sequences of the mitochondrial cytochrome oxidase subunit I gene revealed a substantial haplotype diversity in some populations and high levels of local population structuring in others. Initially, we found mixed evidence of genetic differentiation and connectivity among drainages and populations. Genetic differentiation between the two drainages only became apparent after the Sepirdood population (which belongs to the Caspian Sea drainage) was excluded. Subsequently, the two drainages showed significant genetic distinctions, with a limited gene flow between them. Our demographic analyses supported recent population bottlenecks, followed by a rapid demographic and/or spatial expansion dating back to the Pleistocene climatic fluctuations. Species distribution modelling suggests that precipitation during warm weather conditions profoundly affects the distribution of P. elbursi. This study indicates that freshwater crabs can override short land barriers under favorable weather conditions and will have conservation implications in the face of contemporary climatic fluctuations.