Despite being dominant elements of understory communities in the coniferous forests of western North America, phylogenetic relationships among bilberries (Vaccinium section Myrtillus) remain unresolved. Morphological delimitation among most western bilberry species is tenuous and traditionally employed molecular sources of phylogenetic information have yielded insufficient variability. Moreover, these species are hypothesized to have undergone extensive introgression. We used RADseq data analyzed under maximum likelihood species tree estimation to examine the influence of introgression on relationships among Vaccinium myrtillus, V. scoparium, and V. caespitosum. Additionally, we used these data to assess whether the populations of V. myrtillus disjunct between North America and Eurasia are monophyletic and should continue to be recognized as conspecific. Significant genome-wide introgression, as determined through D-statistic analyses, was detected between North American samples of V. myrtillus and V. caespitosum, and to a lesser extent, between V. myrtillus and V. scoparium. No significant D-values were detected between V. scoparium and V. caespitosum. Accessions of Vaccinium myrtillus from Eurasia and North America were recovered as non-monophyletic, prompting our proposed resurrection of V. oreophilum for North American material. The long-assumed sister species relationship between V. oreophilum and V. scoparium was not recovered in our analysis. Instead, V. oreophilum and V. caespitosum were inferred to be sister taxa. This study reveals considerable introgression detectable in the evolutionary history of western North American bilberries and demonstrates the utility of RADseq data to resolve species level relationships in groups that undergo reticulate evolution such as Vaccinium.