The arrangement of habitat features via historical or contemporary events can strongly influence genomic and demographic connectivity, and in turn affect levels of genetic diversity and resilience of populations to environmental perturbation. The rusty blackbird (Euphagus carolinus) is a forested wetland habitat specialist whose population size has declined sharply (78%) over recent decades. The species breeds across the expansive North American boreal forest region, which contains a mosaic of habitat conditions resulting from active natural disturbance regimes and glacial history. We used landscape genomics to evaluate how past and present landscape features have shaped patterns of genetic diversity and connectivity across the species’ breeding range. Based on reduced-representation genomic and mitochondrial DNA, genetic structure followed four broad patterns influenced by both historical and contemporary forces: (1) an east–west partition consistent with vicariance during the last glacial maximum; (2) a potential secondary contact zone between eastern and western lineages at James Bay, Ontario; (3) insular differentiation of birds on Newfoundland; and (4) restricted regional gene flow among locales within western and eastern North America. The presence of genomic structure and therefore restricted dispersal among populations may limit the species’ capacity to respond to rapid environmental change.