Understanding the driving forces that control vole population dynamics requires identifying bacterial parasites hosted by the voles and describing their dynamics at the community level. To this end, we used high-throughput DNA sequencing to identify bacterial parasites in cyclic populations of montane water voles that exhibited a population outbreak and decline in 2014–2018. An unexpectedly large number of 155 Operational Taxonomic Units (OTUs) representing at least 13 genera in 11 families was detected. Individual bacterial richness was higher during declines, and vole body condition was lower. Richness as estimated by Chao2 at the local population scale did not exhibit clear seasonal or cycle phase-related patterns, but at the vole meta-population scale, exhibited seasonal and phase-related patterns. Moreover, bacterial OTUs that were detected in the low density phase were geographically widespread and detected earlier in the outbreak; some were associated with each other. Our results demonstrate the complexity of bacterial community patterns with regard to host density variations, and indicate that investigations about how parasites interact with host populations must be conducted at several temporal and spatial scales: multiple times per year over multiple years, and at both local and long-distance dispersal scales for the host(s) under consideration.