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Aim: Understanding speciation mechanisms requires disentangling processes that promote and erode population‐level divergence. Three hypotheses are raised that contemporary population structure is mainly shaped by refugial isolation, gene flow or both. Testing these hypotheses requires range‐wide phylogeography and integrative analyses across scales. Here we aimed to (1) re‐estimate the previously unresolved nuclear divergence within a widespread bat; (2) test the above three phylogeographical hypotheses and (3) inform conservation management under climatic change. Location: North America including the Caribbean. Taxon: The big brown bat (Eptesicus fuscus). Methods: We collected range‐wide samples and genome‐wide markers using restriction site‐associated DNA sequencing. Population structure was analysed by clustering methods and spatial estimations. Nuclear phylogeographical divergence was estimated using tree methods (concatenation and coalescence) and network analyses (TreeMix). Phylogeographical hypotheses were tested by comparing alternative evolutionary scenarios using demographic modelling. Species distribution modelling was used to help identify Pleistocene refugia and predict future range shifts under climatic change. Results: We identified three populations in the Caribbean, eastern and western North America. The western population further split into three phylogeographical clades: Pacific, southwestern North America and Mexico. Discordance among mitochondrial and nuclear topologies reflected strong impacts of gene flow without sex bias. Demographic modelling supported scenarios of historical isolation followed by secondary gene flow and estimated Holocene divergence times. Species distribution was essentially continuous during glaciation with possible regional isolation, and northward range shifts were predicted under future climatic change. Main Conclusions: Contemporary population divergence of big brown bats was shaped by both historical isolation and secondary gene flow, supporting the third phylogeographical hypothesis. While climatic change likely triggered initial divergence, ongoing gene flow has largely impacted the dynamic within‐species evolution and generated population divergence without speciation. [ABSTRACT FROM AUTHOR]