Asexual species are thought to suffer more from coevolving parasites than related sexuals. Yet a variety of studies do not find the patterns predicted by theory. Here, to shine light on this conundrum, we investigate one such case of an asexual advantage in the presence of parasites. We follow the frequency dynamics of sexual and asexual Daphnia pulex in a natural pond that was initially dominated by sexuals. Coinciding with an epidemic of a microsporidian parasite infecting both sexuals and asexuals, the pond was rapidly taken over by the initially rare asexuals. With experiments comparing multiple sexual and asexual clones from across the local metapopulation, we confirm that asexuals are less susceptible and also suffer less from the parasite once infected. These results are consistent with the parasite-driven, ecological replacement of dominant sexuals by closely related, but more resistant asexuals, ultimately leading to the extinction of the formerly superior sexual competitor. Our study is one of the clearest examples from nature, backed up by experimental verification, showing a parasite-mediated reversal of competition dynamics. The experiments show that, across the metapopulation, asexuals have an advantage in the presence of parasites. In this metapopulation, asexuals are relatively rare, likely due to their recent invasion. While we cannot rule out other reasons for the observed patterns, the results are consistent with a temporary parasite-mediated advantage of asexuals due to the fact that they are rare, which is an underappreciated aspect of the Red Queen Hypothesis.