The ability to self-fertilize often varies among closely related hermaphroditic plant species, though, variation can also exist within species. In the North American Arabidopsis lyrata, the shift from self-incompatibility (SI) to selfing established in multiple regions independently, mostly since recent postglacial range expansion. This has made the species an ideal model for the investigation of the genomic underpinnings of the breakdown of SI and its population genetic consequences. By comparing nearby selfing and outcrossing populations across the entire species' geographic distribution, we investigated variation at the self-incompatibility (S-)locus and across the genome. Furthermore, a diallel crossing experiment on one mixed-mating population was performed to gain insight in the genetics of mating system variation. We confirmed that the breakdown of SI had evolved in several S-locus backgrounds. The diallel suggested the involvement of binuclearly expressed parental genes with dominance relations. Though, the population-level genome-wide association study did not single out clear-cut candidate genes but several regions with one near the S-locus. On the implication side, selfing as compared to outcrossing populations had less than half of the genomic diversity, while the number of runs of homozygosity and their length scaled with the degree of inbreeding. The results highlight that mating system shifts to selfing, its genetic underpinning and the likely negative genomic consequences for evolutionary potential can be strongly interlinked with past range dynamics.