When confronted with an adaptive radiation, considerable evidence is needed to resolve the evolutionary relationships of these closely related lineages. The North American genus Speyeria is one especially challenging radiation of butterflies due to potential signs of incomplete lineage sorting, ongoing hybridization, and similar morphological characters between species. Previous studies have found species to be paraphyletic and have been unable to disentangle taxa, often due to a lack of data and/or incomplete sampling. As a result, Speyeria remains unresolved. To achieve phylogenetic resolution of the genus, we conducted phylogenomic and population genomic analyses of all currently recognized North American Speyeria species, as well as several subspecies, using restriction-site-associated DNA sequencing (RADseq). Together, these analyses confirm the 16 canonical species, and clarify many internal relationships. However, a few relationships within Speyeria were poorly supported depending on the evolutionary model applied. This lack of resolution among certain taxa corroborates Speyeria is experiencing an ongoing adaptive radiation, with incomplete lineage sorting and lack of postzygotic reproductive barriers contributing to hybridization and further ambiguity. Given that many Speyeria taxa are under duress from anthropogenic factors, their legal protection must be viewed cautiously and on a case by case basis in order to properly conserve the diversity being generated.