Bacterial communities associated with animals show complex spatial and temporal variation. The main driving forces behind this variation are still to be deciphered. Differences in microbiome composition could be caused by stochastic changes, such as random gain and loss of microbiome components, as well as deterministic factors, such as variation in temperature (or other abiotic factors), diet, or the availability of microbes with the potential to colonize the hosts in the surrounding environment. Here we investigated seasonal variation in the microbiome of Hydra polyps and the bacterioplankton surrounding them to test the hypothesis that the contribution of environmental microorganisms to host-associated microbial communities varies seasonally. Sampling was performed for two consecutive years in three distinct temperate water bodies in Eastern Hungary: a shallow lake, a deep lake, and a river. We found that the microbiomes of polyps differed from their surrounding environment and varied seasonally. The similarity of polyp and water microbiomes changed seasonally in a population-specific way: microbial communities associated with polyps became markedly more similar to that of their surrounding environment during the summer in the shallow lake habitat, but not in the other populations. Our results suggest that environmental and host-associated microbiomes change independently during most of the year, but high temperature increases the impact of environmental microbiome on host-associated microbial communities.