The epidermal mucus layer has established importance to fish systems, but there is an evident gap in knowledge of the microbial community’s structure and function (‘microbiome’) inhabiting fish skin, particularly in freshwater. In general, we know that the microbiome of other are organs, such as the gut, are essential to host health and provide protection from parasites by priming the immune system before invasion. Like gut microbiomes, the skin microbiome contains mutualistic and commensal microbes adapted to the epidermal surface, and these are affected by environmental and host species-dependent factors. We tested whether the microbiome present on the host pre-infection could predict subsequent infection susceptibility to an ectoparasitic helminth. Using 16S rRNA analysis, we studied the bacterial communities of Trinidadian guppies (Poecilia reticulata) and their interaction with Gyrodactylus turnbulli. Gyrodactylus parasites are ubiquitous monogenean ectoparasites that infect the skin and gills of teleost fish in marine and freshwater ecosystems. We swabbed fish skin to inventory the skin microbiome before experimentally infecting them with G. turnbulli. We found that fish skin microbiome communities can predict infection severity. Additionally, we found that male and female guppies differed in their alpha diversity before infection with G. turnbulli, their defense against the parasites, and their behavior. Our results, therefore, suggest that the fish skin microbiome alters the host-parasite interactions during Gyrodactylus infection, ultimately changing parasite load, thus presumably mortality and transmission. Future experiments will test how environmental factors may alter the skin microbiome, improve or worsen infection outcomes for the host, and how parasites may respond to changing microbial communities.