We collected Oropsylla montana from rock squirrels, Spermophilus varigatus, and infected a subset of collected fleas with Yersinia pestis, the etiological agent of plague. We used bar-tagged DNA pyrosequencing to characterize bacterial communities of wild, uninfected controls and infected fleas. Bacterial communities within Y. pestis-infected fleas were substantially more similar to one another than communities within wild or control fleas, suggesting that infection alters the bacterial community in a directed manner such that specific bacterial lineages are severely reduced in abundance or entirely eliminated from the community. Laboratory conditions also significantly altered flea-associated bacterial communities relative to wild communities, but much less so than Y. pestis infection. The abundance of Firmicutes decreased considerably in infected fleas, and Bacteroidetes were almost completely eliminated from both the control and infected fleas. Bartonella and Wolbachia were unaffected or responded positively to Y. pestis infection.