While host-species diversity often influences microbial prevalence, there may be multiple mechanisms causing such effects that may also depend on the foraging strategy of the microbes. We employed a natural gradient of rodent-species richness to examine competing hypotheses describing possible mechanisms mediating the relationship between host-species richness and the prevalence of the most dominant microbes, along with microbe specificity to the different rodent host species. We sampled blood from three gerbil species in plots differing in terms of the proportion of the different species and screened for the most dominant bacteria. Two dominant bacterial lineages were detected: host-specific bacteria and host-opportunistic bacteria. Using a model selection approach, we detected evidence for both direct and indirect effects of host-species richness on the prevalence of these bacteria. Infection probability of the host-specific lineage was lower in richer host communities, most likely due to increased frequency and density of the least suitable host species. In contrast, field observations suggest that the effect of host-species richness on infection probability of the opportunistic lineage was both direct and indirect, mostly mediated by changes in flea densities on the host and by the presence of the host-specific lineage. Our results thus suggest that host-species richness has multiple effects on microbial prevalence, depending on the degree of host-specificity of the microbe in question.