Although the genetic consequences of contemporary landscape composition and range shifts driven Pleistocene climatic oscillations have been studied fairly well in alpine organisms, we know much less about how these factors have shaped the demography of taxa with broader climatic niches and distributions. Here, we use high-throughput sequencing data to study the processes underlying spatial patterns of genomic variation in Omocestus panteli (Bolívar, 1887) (Orthoptera: Acrididae), a common Iberian grasshopper distributed across numerous habitat types and a wide elevational range (from sea level to >2,000 m). Although the species is broadly distributed, our analyses support that its contemporary populations show significant genetic fragmentation that dates back to the last glacial period. Accordingly, spatially explicit testing of alternative gene flow scenarios and demographic inference analyses revealed that genetic differentiation between populations and their long-term effective population sizes are best explained by the spatial configuration of environmentally suitable habitats during the last glacial maximum (ca. 21 ka). At that time, the species experienced net demographic expansions but interspersed unsuitable areas might have disrupted gene flow and created opportunity for geographical diversification. Collectively, our analyses indicate that the genetic makeup of contemporary populations is not well explained by current environmental factors or geographical barriers to dispersal but mostly reflects genetic fragmentation during the last glacial period followed by postglacial admixture among previously isolated gene pools. Taken together, these results support that the Pleistocene ‘species pump’ model might be also useful in explaining demographic dynamics and geographical diversification in taxa characterized by broad climatic niches.