The level of gene flow between diverging lineages ultimately determines the outcome of a speciation event. If secondary contact occurs before this process is complete, reproductive isolation barriers must exist or evolve to prevent hybridization. The selective pressures facilitating and maintaining genetic divergence do not always involve an observable phenotypic response, thus cryptic species form. The inability to distinguish between sibling species can be a particularly serious problem in groups responsible for pathogen transmission. Culicoides biting midges occur almost world-wide and vector many disease-causing pathogens that affect wildlife and livestock. In North America, the C. variipennis species complex contains three currently recognized species, only one of which is a vector, and limited molecular and morphological differences have hindered vector surveillance. Here, genomic methods were used to investigate speciation and genetic structure within this complex. Single nucleotide polymorphism (SNP) data were generated using ddRAD sequencing for 206 individuals originating from 17 locations throughout the United States and Canada. Clustering analyses consistently suggest the occurrence of five putative species with significant differentiation occurring in both sympatric and allopatric populations. Evidence of hybridization was detected in three different species pairings, indicating a lack of pre-zygotic reproductive isolation within the complex. Mitochondrial genes were used to trace the hybrid parentage of these individuals, which illuminated discordance with the SNP data. In this study, we highlight the potential role of geographic, ecological, and behavioral isolation in speciation and in maintaining species boundaries, despite hybridization and long range dispersal.