Our understanding of how microbiome signatures are modulated in wild fish populations remains poorly developed and has, until now, mostly been inferred from studies in commercial and farmed fish populations. Here, for the first time, we have studied changes in the skin and blood microbiomes of the Salmo trutta population of the volcanic Kerguelen archipelago located at the northern limit of the Antarctic Ocean. The Kerguelen Islands present a natural framework of population expansion and reveal a likely situation representing further climate change in distribution areas. Our results showed that S. trutta of the Kerguelen Islands has a microbiome signature distinct from those of salmonids of the Northern Hemisphere. Our study also revealed that the skin and blood microbiomes differ between sedentary and migratory S. trutta. While 18 phyla were shared between both groups of trout, independent of the compartment, 6 phyla were unique to migratory trout. Further analyses showed that microbiome signatures undergo significant site-specific variations that correlate, in some cases, with the peculiarity of specific ecosystems. Our study also revealed the presence of potential pathogens at particular sites and the impact of abiotic factors on the microbiome, most notably due to the volcanic nature of the environment. This study contributes to a better understanding of the factors that modulate the microbiome signatures of migratory and sedentary fish populations. It will also help to better monitor the impacts of climate change on the colonization process in the sub-Antarctic region.