Holarctic species offer great opportunities to study biogeography, phylogenetics, taxonomy, and local adaptation. Species that are considered conspecific between the Palearctic and the Nearctic realms are often split into 2 or more species when denser sampling and molecular markers are applied. Similar in complexity but at a finer geographical scale are species groups having Arctic-Alpine distributions where lineages have complicated demographic histories due to glacial dynamics. In both cases, allopatric speciation might not result in fast differentiation of morphological characters if environmental conditions in isolated areas are similar and the main driver of variability is genetic drift. Here, we study the Holarctic Pardosa hyperborea (Thorell, 1872) and its closest European relatives to assess their taxonomic status and patterns of genetic variability. Based on DNA barcodes and genomic data from double-digest restriction site associated sequencing, we propose that the North American populations should be regarded as a distinct species (P. luteola Emerton,1894, stat. resurr.), possibly consisting of several independent lineages. With the help of D-statistics, population genetic simulations and phylogenetic networks analysis, we demonstrate historical introgression among European species of the group and a likely explanation for shared DNA barcodes among allopatric and fully differentiated species. Our study exposes a promising model for studying speciation processes and demographic history in parallel on both sides of the Atlantic Ocean and demonstrates the usefulness of genomic tools in elucidating the taxonomy and biogeography of taxa across broad geographic scales.