Species distributions are often indicative of historical biogeographical events and contemporary spatial biodiversity patterns. The Harlequin Duck Histrionicus histrionicus is a sea duck of conservation concern that has a disjunct distribution, with discrete portions of its range associated with northern Pacific and Atlantic Ocean basins. Movement data indicate migratory connectivity within regions of each ocean basin but not cross-continent dispersal, suggesting that genetic structuring could exist at multiple spatial scales. Little is known regarding the impacts of past vicariance events on the species phylogeographical structure and historical demography, or rates of gene flow at different spatial scales. We used data from microsatellite loci and mitochondrial DNA (mtDNA) sequences to quantify levels of genetic diversity within, and the extent of spatial genetic differentiation among locations sampled at multiple spatial scales across the species range. Samples were collected at nonbreeding locations, which represent groupings appropriate for characterizing genetically differentiated subgroups at regional and continental scales. Collectively, genetic data and coalescence modelling suggested that individuals colonized regions currently occupied within both ocean basins in the Holocene from a single refuge in the Atlantic. Further, it seems likely there was secondary contact with lineages derived from populations in Asia, based on the shallow species-wide mtDNA phylogeny and high incidence of recently derived private mtDNA haplotypes. Estimates of inter-location variance in microsatellite allele and mtDNA haplotype frequency were moderate and significant between western (Pacific – North America) and eastern (Atlantic – North America, Greenland and Iceland) ocean basins and among sampling groups within each ocean basin. Genetic differentiation among sampling groups was particularly evident at the species distributional margins in the Atlantic (Iceland) and the Pacific (Shemya Island) Ocean basins. Coalescent modelling results suggest that contemporary spatial genetic patterns in the species arose through the combined influences of secondary contact, shared ancestry and gene flow after the last glacial maxima.