Fertilization proteins of marine broadcast spawning species often show signals of positive selection. Among geographically isolated populations, positive selection within populations can lead to differences between them, and may result in reproductive isolation upon secondary contact. Here, we test for positive selection in the reproductive compatibility locus, bindin, in two populations of a sea star on either side of a phylogeographic break. We find evidence for positive selection at codon sites in both populations, which are under neutral or purifying selection in the reciprocal population. The signal of positive selection is stronger and more robust in the population where effective population size is larger and bindin diversity is greater. In addition, we find high variation in coding sequence length caused by large indels at two repetitive domains within the gene, with greater length diversity in the larger population. These findings provide evidence of population-divergent positive selection in a fertilization compatibility locus, and suggest that sexual selection can lead to reproductive divergence between conspecific marine populations.