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Abstract Background Biogeography has been linked to differences in gut microbiota in several animals. However, the existence of such a relationship in fish is not clear yet. So far, it seems to depend on the fish species studied. However, most studies of fish gut microbiotas are based on single populations. In this study, we investigated the gut microbiota of fish from three wild populations of the two-banded sea bream Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) to determine whether its diversity, structure and potential functionality reflect the geographic origin of the fish, at large and small geographical scale. Additionally, we explored the host- and environmental-related factors explaining this relationship. Results We showed that the taxonomy and potential functionality of the mucosa-associated gut microbiota of Diplodus vulgaris differ to varying degrees depending on the spatial scale considered. At large scale, we observed that both the taxonomical structure and the potential functionality of the fish microbiota differed significantly between populations. In contrast, the taxonomical diversity of the microbial community displayed a significant relationship with factors other than the geographic origin of the fish (i.e. sampling date). On the other hand, at small scale, the different composition and diversity of the microbiota differ according to the characteristics of the habitat occupied by the fish. Specifically, we identified the presence of Posidonia oceanica in the benthic habitat as predictor of both the microbiota composition and diversity. Lastly, we reported the enrichment of functions related to the metabolism of xenobiotics (i.e. drugs and 4-aminobenzoate) in a population and we indicated it as a potential target of future monitoring. Conclusions With this study, we confirmed the importance of investigating the gut microbiota of wild fish species using multiple populations, taking into account the different habitats occupied by the individuals. Furthermore, we underscored the use of the biodegradation potential of the gut microbiota as an alternative means of monitoring emerging contaminants in Mediterranean fish.