The transition from water to air, or terrestrialization, is a key event in the evolution of many marine organisms to exploit new ecological niches for food, stress buffers, and to access higher and temperature-independent air oxygen concentrations. Microorganisms are pivotal for host adaptation, however their contribution to overcoming the challenges posed by the lifestyle changes from water to land is not well understood. In this study, we examined how microbial associations with a key multifunctional organ, the gill, is involved in the intertidal adaptation of mangrove dwelling fiddler crabs, which are dual-breathing organisms. Electron microscopy revealed a rod-shaped bacterial layer tightly connected to the gill lamellae of five crab species sampled across a latitudinal gradient spanning the central Red Sea to the southern Indian Ocean. The gill bacterial community diversity assessed with 16S rRNA gene amplicon sequencing was consistently low across crab species, and the same actinobacterial group, namely Ilumatobacter, was dominant regardless of the geographic location of the host. Using metagenomics and metatranscriptomics, these members of actinobacteria were found to potentially be able to convert ammonia to amino acids and could help eliminate the toxic sulphur compounds and carbon monoxide to which crabs are constantly exposed. These results indicate that gill bacteria can play a role in the adaptation of animals in dynamic intertidal ecosystems. Hence, this relationship is likely to be important in the ecological and evolutionary processes of the transition from water to air and deserves further attention, including the ontogenetic onset of this association.