Models of host-parasite coevolution predict pronounced genetic dynamics if resistance and infectivity are genotype-specific or associated with costs, and if selection is fueled by sufficient genetic variation. We addressed these assumptions in the black bean aphid, Aphis fabae, and its parasitoid Lysiphlebus fabarum. Parasitoid genotypes differed in infectivity and host clones exhibited huge variation for susceptibility. This variation occurred at two levels. Clones harboring Hamiltonella defense, a bacterial endosymbiont known to protect pea aphids against parasitoids, enjoyed greatly reduced susceptibility, yet clones without H. defensa also exhibited significant variation. Although there was no evidence for genotype-specificity in the H. defensa-free clones' interaction with parasitoids, we found such evidence in clones containing the bacterium. This suggests that parasitoid genotypes differ in their ability to overcome H. defensa, resulting in an apparent host × parasitoid genotype interaction that may in fact be due to an underlying symbiont × parasitoid genotype interaction. Aphid susceptibility to parasitoids correlated negatively with fecundity and rate of increase, due to H. defensa-bearing clones being more fecund on average. Hence, possessing symbionts may also be favorable in the absence of parasitoids, which raises the question why H. defensa does not go to fixation and highlights the need to develop new models to understand the dynamics of endosymbiont-mediated coevolution.