The need for reproductive assurance during dispersal, along with the pressure of local mate competition, means that the importance of frequent or repeated colonization is implicit in the literature on sexual system evolution. However, there have been few empirical tests of the association between colonization history and sexual system in plants, and none within a single species. Here we use patterns of genetic diversity to provide such a test in the Mercurialis annua species complex, which spans the range of systems from self-compatible monoecy through androdioecy to dioecy. This variation has been hypothesized to result from differing patterns of metapopulation turnover and recolonization. Because monoecy should be favored during colonization, androdioecy and dioecy will be maintained only in regions with low rates of local extinction and recolonization, and these differences should also be reflected in patterns of neutral genetic diversity. We show that monoecious populations of M. annua display lower within-population genetic diversity than androdioecious populations and higher genetic differentiation than dioecious and androdioecious populations, as predicted by metapopulation models. In contrast, regional diversity in M. annua appears to be primarily a product of postglacial range expansion from two refugia in the eastern and western Mediterranean Basin.