Reproductive barriers drive divergence by restricting gene flow between populations. However, barriers are often semipermeable, allowing some gene flow between groups. Further, populations may vary in the number and coincidence of reproductive barriers. This dissertation focuses on patterns of gene exchange among populations of European corn borer moths (Ostrinia nubilalis) that vary in the number of acting barriers. In Chapter One, I performed an empirical test of a ‘coupling hypothesis’ of reproductive barriers, which examines how their joint effects enhance reproductive isolation and genomic divergence. I found divergence mainly restricted to barrier loci when populations differ by a single barrier, whereas the coincidence of temporal and behavioral barriers is associated with enhanced divergence. Specifically, differentiation at temporal barrier loci increases in the presence of behavioral divergence and differentiation at behavioral barrier loci increases in the presence of temporal divergence. In Chapter Two, I examine how barrier loci can guide life history variation when a species expands its range. To identify whether the genome reflects signatures of natural selection at such phenological loci, I studied the genomes of moths from populations along a latitudinal gradient in the Midwestern US. I found genome-wide signatures that were reflective of a large expansion in both range and population size and demonstrated that two key life history loci showed signatures consistent with both selection and demographic processes. Finally, in Chapter Three, I considered how introgression and recombination complicate patterns of ancestry of key barrier loci, using genealogical trees for individuals and species of the Ostrinia moth group. I developed tree sequence topologies from both genome wide markers and a set of four barrier trait loci and calculated genealogical nearest neighbor estimates, a statistic summarizing relative ancestry proportions of each individual to describe how phenotypic variation has shaped the species and population history of O. nubilalis. I showed that much of the genome reflects genealogical sharing across many populations, but genealogies at barrier loci distinguish groups. Finally, there was evidence of introgression of these barrier traits between multiple species within the Ostrinia group, suggesting a complex model for barrier trait evolution in this group.