Symbiotic microorganisms may provide their hosts with abilities critical to their occupation of microhabitats. Gut (intestinal) bacterial communities aid animals to digest substrates that are either innutritious or toxic, as well as support their development and physiology. The role of microbial communities associated with sibling species in the hosts’ adaptation remains largely unexplored. In this study, we examined the composition and plasticity of the bacteriomes in two sibling intertidal gastropod species, Littorina fabalis and L. obtusata, which are sympatric but differ in microhabitats. We applied 16S rRNA gene metabarcoding and shotgun sequencing to describe associated microbial communities and their spatial and temporal variation. A significant drop in the intestinal bacteriome diversity was revealed during the cold season, which may reflect temperature-related metabolic shifts and changes in snail behavior. Importantly, there were significant interspecies differences in the gut bacteriome composition in summer but not in autumn. The genera Vibrio, Aliivibrio, Moritella and Planktotalea were found to be predominantly associated with L. fabalis, while Granulosicoccus, Octadecabacter, Colwellia, Pseudomonas, Pseudoalteromonas and Maribacter were found to be mostly associated with L. obtusata. Based on these preferential associations, we analyzed the metabolic pathways’ enrichment. We hypothesized that the L. obtusata gut bacteriome contributes to decomposing algae and detoxifying polyphenols produced by fucoids. Thus, differences in the sets of associated bacteria may equip their closely phylogenetically related hosts with a unique ability to occupy specific micro-niches.