Facultative symbionts are widespread in arthropods and can provide important services such as protection from natural enemies. Yet what shapes associations with defensive symbionts in nature remains unclear. Two hypotheses suggest that interactions with either antagonists or host plants explain the prevalence of symbionts through shared selective pressures or vectors of symbiont transmission. Here we investigate the factors determining similarities in the Hamiltonella defensa symbiosis shared amongst field-collected aphid species. After accounting for host species relatedness, we find that Hamiltonella's genotype distribution aligns with sharing the same parasitoids, rather than host plants, highlighting parasitoids and hosts as key selective agents shaping the symbiosis across aphid species. Our data indicates parasitoid host specificity drives the prevalence of specific aphid-Hamiltonella associations, suggesting defensive symbioses are maintained by the selective pressure imposed by dominant parasitoids and their aphid hosts. These findings underscore the importance of interactions with natural enemies in explaining patterns of defensive symbiosis in nature.