Interactions with parasites may promote the evolution of disassortative mating in host populations as a mechanism through which genetically diverse offspring can be produced. This possibility has been confirmed through simulation studies and suggested for some empirical systems in which disassortative mating by disease resistance genotype has been documented. The generality of this phenomenon is unclear, however, because existing theory has considered only a subset of possible genetic and mating scenarios. Here we present results from analytical models that consider a broader range of genetic and mating scenarios and allow the evolution of non-random mating in the parasite as well. Our results confirm results of previous simulation studies, demonstrating that coevolutionary interactions with parasites can indeed lead to the evolution of host disassortative mating. However, our results also show that the conditions under which this occurs are significantly more fickle than previously thought, requiring specific forms of infection genetics and modes of non-random mating that do not generate substantial sexual selection. In cases where such conditions are not met, hosts may evolve random or assortative mating. Our analyses also reveal that coevolutionary interactions with hosts cause the evolution of non-random mating in parasites as well. In some cases, particularly those where mating occurs within groups, we find that assortative mating evolves sufficiently to catalyze sympatric speciation in the interacting species.