Summary Mating system transitions from self‐incompatibility (SI) to self‐compatibility (SC) are common in plants. In the absence of high levels of inbreeding depression, SC alleles are predicted to spread due to transmission advantage and reproductive assurance. We characterized mating system and pistil‐expressed SI factors in 20 populations of the wild tomato species Solanum habrochaites from the southern half of the species range. We found that a single SI to SC transition is fixed in populations south of the Rio Chillon valley in central Peru. In these populations, SC correlated with the presence of the hab‐6 S‐haplotype that encodes a low activity S‐RNase protein. We identified a single population segregating for SI/SC and hab‐6. Intrapopulation crosses showed that hab‐6 typically acts in the expected codominant fashion to confer SC. However, we found one specific S‐haplotype (hab‐10) that consistently rejects pollen of the hab‐6 haplotype, and results in SI hab‐6/hab‐10 heterozygotes. We suggest that the hab‐10 haplotype could act as a genetic mechanism to stabilize mixed mating in this population by presenting a disadvantage for the hab‐6 haplotype. This barrier may represent a mechanism allowing for the persistence of SI when an SC haplotype appears in or invades a population.