ABSTRACTMicrobes contribute to aquatic ecosystem function and the fitness of macroscopic organisms, including zooplankton. Many factors affect the taxonomic compositions of free‐living (bacterioplankton) and zooplankton‐associated microbial communities in lakes; yet how these communities vary seasonally and among lakes remains poorly understood. Here, we investigate how free‐living bacterial communities and those associated with different crustacean zooplankton hosts change in response to fluctuations in their natural environment across time and space. We repeatedly sampled bacterioplankton, zooplankton communities, zooplankton microbiomes, and water chemistry parameters of six lakes in the eastern Sierra Nevada mountains of California across a summer season. 16S rRNA gene sequencing revealed clear differences in the community composition and relative abundance of bacterial taxa between bacterioplankton and zooplankton microbiomes, which was best explained by lake and host identity rather than intraseasonal sampling times. Bacterioplankton communities were highly conserved across the summer season and showed higher alpha diversity, but lower species turnover, than zooplankton microbiomes, which were more variable and largely partitioned by host taxa and phylogenetics (Copepoda vs. Cladocera). Spatial and local environmental context (drainage basin, home‐lake habitat) interacted secondarily with community types (free‐living, host‐associated) and zooplankton host identity to shape bacterial community composition. These results show that deterministic processes related to host filtering, host taxonomy, and spatial/environmental variation among lakes drive changes in microbial communities more than temporal changes within lakes. Higher beta diversity among zooplankton‐associated microbes suggests dispersal limitation and/or local selection play stronger roles for zooplankton microbiomes than for free‐living bacterioplankton.