AbstractAimGlacial‐interglacial cycles influenced the contemporary genetic structure of many North American species. While phylogeographical lineage divergence among Pleistocene refugia has been proposed as a significant driver of subspecific and ecotypic differentiation, emerging evidence highlights the role of diversification within refugia in producing post‐glacial variation. Caribou (Rangifer tarandus) exhibit significant morphological, ecological and behavioural phenotypic variation and occurred within Beringian and sub‐Laurentide refugia. More specifically, the boreal ecotype of woodland caribou ranges from the southern regions of Canada to the Northwest Territories (NWT). Woodland caribou are generally accepted to have evolved south of the glacial extent, but the boreal ecotype in the northern part of their range co‐occurs with caribou that have a Beringian origin. This proximity provides an opportunity to test whether woodland caribou colonized boreal habitats from a single southern refugial source or if independent evolution to a common ecotype resulted from diversification within refugia.LocationNorthwestern Canada.MethodsWe used approximate Bayesian computation to discriminate between alternate evolutionary histories of caribou belonging to boreal, northern mountain and barren‐ground ecotypes using microsatellite and mtDNA markers.ResultsOur analysis indicates that unlike the southern‐evolved boreal ecotype, the boreal ecotype of central NWT has Beringian origins and arose from a common lineage with barren‐ground and mountain caribou. Importantly, the divergence of the lineage resulting in the boreal ecotype of central NWT significantly pre‐dates the Last Glacial Maximum.Main conclusionsWe demonstrate that independent evolutionary trajectories can converge on a similar phenotype and for the first time show that the boreal ecotype of caribou in North America contains two phylogeographical assemblages. The ancient divergence suggests that diversification within Beringia could have resulted in ecological specialization. An eco‐evolutionary focus will be essential to designing biodiversity conservation strategies for caribou that maximize genetic diversity and preserve adaptive potential in this intraspecifically diverse species.