Arabidopsis lyrata is mostly outcrossing due to a sporophytic self-incompatibility (SI) system but around the Great Lakes of North America some populations have experienced a loss of SI. We researched the loss of SI in a phylogeographic context. We used cpDNA and microsatellite markers to test if populations of North-American A. lyrata around the Great Lakes have experienced different (recent) histories, and linked this with individually established selfing phenotype and population level realized outcrossing rates calculated based on variation in progeny arrays at multi-locus microsatellite markers. We found three chloroplast haplotypes, in two of which the loss of self-incompatibility had occurred independently. Shifts to high rates of inbreeding were most apparent in one of these lineages but individuals showing loss of SI occurred in all three. Self-compatible individuals usually showed a reduction of observed heterozygosity (HO) compared to outcrossing individuals. In the lineage that included the populations with the highest levels of inbreeding, this reduction was more substantial. This may indicate that the loss of SI in this lineage did not occur as recently as in the other lineage. The geographic distribution of the haplotypes suggested that there had been at least two independent colonization routes to the north of the Great Lakes following the last glaciation. This is consistent with postglacial migration patterns that have been suggested for other organisms with limited dispersal, such as reptiles and amphibians.