The freshwater isopod Asellus aquaticus is an important decomposer of leaf detritus, and its diverse gut microbiome has been depicted as key contributors in lignocellulose degradation as of terrestrial isopods. However, it is not clear whether the individual-level microbiome profiles in the isopod digestive system across different habitats match the implied robust digestion function of the microbiome. Here, we described the bacterial diversity and abundance in the digestive system (hindgut and caeca) of multiple A. aquaticus individuals from two contrasting freshwater habitats. Individuals from a lake and a stream harboured distinct microbiomes, indicating a strong link between the host-associated microbiome and microbes inhabiting the environments. While faeces likely reflected the variations in environmental microbial communities included in the diet, the microbial communities also substantially differed in the hindgut and caeca. Microbes closely related to lignocellulose degradation are found consistently more enriched in the hindgut in each individual. Caeca often associated with taxa implicated in endosymbiotic/parasitic roles (Mycoplasmatales and Rickettsiales), highlighting a complex host-parasite-microbiome interaction. The results highlight the lability of the A. aquaticus microbiome supporting the different functions of the two digestive organs, which may confer particular advantages in freshwater environments characterized by seasonally fluctuating and spatially disparate resource availability.