All animals harbor a community of microbial endosymbionts that play integral roles in organismal function.  Here, we use more than 350 16S rDNA sequences to investigate the symbiotic bacterial communities of three flea species known to be vectors of bacterial diseases: Oropsylla hirsuta, Oropyslla montana, and Xenopsylla cheopis. We find that the diversity of bacteria associated with fleas is relatively low. However, while overall community diversity is low, the bacterial community composition differs greatly among individual fleas. Communities within individual fleas do not randomly assemble from the regional species pool. Instead, individual fleas tend to be dominated by one bacterial lineage. Inter-specific competition, precedence effects related to the timing of colonization, or pulses of nutrients may explain the dominance of a single lineage.  We find that the transmission strategy of the bacterial lineage (vertical or horizontal) affects its distribution.  The same strain of Bartonella, a horizontally transmitted lineage, is found in both Oropsylla species, but each flea species harbors its own very divergent lineage of the vertically transmitted Rickettsiales.  Finally, we use population genetic analyses of DNA sequences from the dominant lineages and infer migration rates, effective population sizes, and population growth patterns.  Our findings shed light on the generation of variation within a bacterial population and on the evolution of bacterial disease agents.