AbstractThe systematics of Speyeria butterflies has historically been complicated by intraspecific variability that has challenged efforts to delimit species and reconstruct phylogenies. Our study presents a phylogenetic comparison of genomic single nucleotide polymorphisms (SNPs) and mitochondrial COI gene sequences, with comprehensive taxon sampling that includes 15 species and 46 subspecies. Increased sampling of genetic markers and taxa improved the match between genetic clusters, obtained with both phylogenetic and cluster‐based analyses, and species previously detected using morphology, as well as showing two species delimitations that may need revision. We also recovered extensive mitonuclear discordance between genomic SNPs and the COI gene, confirming that mitochondrial DNA does not reliably identify several species at broad geographic scales. Resolution of the relationships of Speyeria species demonstrates the importance of sampling variation across the whole genome, and provides an essential foundation for understanding the evolution of this charismatic clade of North American butterflies.