In recently diverged species, ancestral polymorphism and introgression can cause incongruence between gene and species trees. In the face of hybridization, few genomic regions may exhibit reciprocal monophyly, and these regions, usually evolving rapidly under selection, may be important for the maintenance of species boundaries. In animals with internal fertilization, genes encoding seminal protein are candidate barrier genes. Recently diverged hybridizing species such as the field crickets Gryllus firmus and G. pennsylvanicus, offer excellent opportunities to investigate the origins of barriers to gene exchange. These recently diverged species form a well-characterized hybrid zone, and share ancestral polymorphisms across the genome. We analyzed DNA sequence divergence for seminal protein loci, housekeeping loci, and mtDNA, using a combination of analytical approaches and extensive sampling across both species and the hybrid zone. We report discordant genealogical patterns and differential introgression rates across the genome. The most dramatic outliers, showing near-zero introgression and more structured species trees, are also the only two seminal protein loci under selection. These are candidate barrier genes with possible reproductive functions. We also use genealogical data to examine the demographic history of the field crickets and the current structure of the hybrid zone.