The Arctic tundra biome is undergoing rapid shrub expansion (“shrubification”) in response to anthropogenic climate change. During the previous ~2.6 million years, glacial cycles caused substantial shifts in Arctic vegetation, leading to changes in species’ distributions, abundance, and connectivity, which have left lasting impacts on the genetic structure of modern populations. Examining how shrubs responded to past climate change using genetic data can inform the ecological and evolutionary consequences of shrub expansion today. Here we test scenarios of Quaternary population history of dwarf birch species (Betula nana L. and Betula Glandulosa Michx.) using SNP markers obtained from RAD sequencing and approximate Bayesian computation. We compare the timings of population events with ice sheet reconstructions and other paleoenvironmental information to untangle the impacts of alternating cold and warm periods on the phylogeography of dwarf birch. Our best supported model suggested that the species diverged in the Mid-Pleistocene Transition as glaciations intensified, and ice sheets expanded. We found support for a complex history of inter- and intraspecific divergences and gene flow, with secondary contact occurring during periods of both expanding and retreating ice sheets. Our spatiotemporal analysis suggests that the modern genetic structure of dwarf birch was shaped by transitions in climate between glacials and interglacials, with ice sheets acting alternatively as a barrier or an enabler of population mixing. Tundra shrubs may have had more nuanced responses to past climatic changes than phylogeographic analyses have often suggested, with implications for future eco-evolutionary responses to anthropogenic climate change.