A common strategy of pathogenic bacteria is to form close associations with parasitic insects that feed on animals and to use these insects as vectors for their own transmission. Pathogens interact closely with other coexisting bacteria within the insect, and interactions between co-occurring bacteria may influence the vector competency of the parasite. Interactions between particular lineages can be explored through measures of alpha-diversity. Furthermore, general patterns of bacterial community assembly can be explored through measures of beta-diversity. Here, we use pyrosequencing (n=115,924 16S rRNA gene sequences) to describe the bacterial communities of 230 prairie dog fleas sampled across space and time. We use these communinty characterizations to assess interactions between dominant community members and to explore general patterns of bacterial community assembly in fleas. An analysis of co-occurrence patterns suggests non-neutral negative interactions between dominant community members (P<0.001). Furthermore, bacterial communities of fleas shift dramatically across years (phylotype-based: R=0.829, P<0.001; phylogenetic-based: R=0.612-0.753, P<0.001), but they also significantly differ across space (phylotype-based: R=0.418, P<0.001; phylogenetic-based: R=0.290-0.328, P<0.001) and between flea species (phylotype-based: R=0.160, P=0.011; phylogenetic-based: not significant). Collectively, our results show that flea-associated bacterial communities are not random assemblages; rather, an individual flea's bacterial community is governed by interactions between bacterial lineages and by the flea's place in space and time.