The microbiome – the community of microorganisms that is associated with an individual animal – has been an important driver of insect biodiversity globally, enabling insects to specialize on narrow, nutrient deficient diets. The importance of maternally inherited, obligate bacterial endosymbionts to provisioning nutrients missing from these narrow dietary niches has been well studied in insects. However, we know comparatively little about the processes that dictate the composition of non-maternally inherited bacteria in insect microbiomes, despite the importance of these bacteria in insect health, fitness, and vector competence. Here, we used two species of obligate insect ectoparasites of bats, the bat flies (Streblidae) Trichobius sphaeronotus and Nycterophilia coxata, to examine whether the microbiome, beyond obligate bacterial endosymbionts, is conserved or variable across geographic space, between ectoparasite species, or covaries with the external microbiome of their bat hosts or the cave environment. Our results indicate that ectoparasite microbiomes are highly conserved and specific to ectoparasite species, despite these species feeding on the blood of the same bat individuals in some cases. In contrast, we found high geographic variation in the fur microbiome of host bats and that the bat fur microbiome mimics the cave microbiomes. This research suggests that there is constraint on blood-feeding insect ectoparasites to maintain a specific microbiome distinct from their host and the environment, potentially to meet their nutritional needs. Given many of these bacteria are not known to be maternally inherited, this research lays the foundation for future examinations of how blood-feeding arthropods acquire and maintain bacteria in their microbiomes.