Arabidopsis lyrata has become a useful system for the study of comparative genomics, hybridization, polyploidyization, and evolutionary transitions from outcrossing to selfing. Previous studies of its mating system have used microsatellite loci but low allelic diversity, particularly in self-compatible populations characterized by low levels of outcrossing, reduce these markers for more detailed studies. Here, we aimed to develop population-level SNP markers for A. lyrata ssp. lyrata. We performed de novo SNP discovery and identified 6,808 putative SNPs from genome-wide sequences of 22 individuals originating from a highly selfing population. Further filtering and marker validation enabled the development of 17 SNP marker loci that can be visualized using standard PCR-RFLP protocols. These markers had average minor-allele frequencies of 0.40 in the target population and four of seven markers were variable in a small sample from nine other A. lyrata populations. These PCR-RFLP markers have the potential to be useful for the analysis of mating patterns in within and beyond the inbred self-compatible populations of A. lyrata studied here, and enable the continued development of A. lyrata as a model for studying evolutionary transitions from outcrossing to selfing.