Predicting the effects of global increase in temperatures on disease virulence is challenging, especially for environmental opportunistic bacteria, because pathogen fitness may be differentially affected by temperature within and outside host environment. So far, there is very little empirical evidence on the connections between optimal temperature range and virulence in environmentally growing pathogens. Here we explored if the virulence of an environmentally growing opportunistic fish pathogen, Flavobacterium columnare, is malleable to evolutionary changes via correlated selection on thermal tolerance. To this end, we experimentally quantified the thermal performance curves (TPCs) for maximum biomass of 49 F. columnare isolates from eight different geographic locations in Finland over ten years (2003-2012). We also characterized virulence profiles of these strains in a zebra-fish (Danio rerio) infection model. We show that virulence among the strains increased over the years, but tolerance to higher temperatures was negatively associated with virulence. Our data suggest that temperature has a strong effect on the pathogen genetic diversity, and therefore presumably also on disease dynamics. However, the observed increase in frequency and severity of F. columnare epidemics over the last decade cannot be directly linked to bacterial evolution due to increased mean temperature, but is most likely associated with factors related to increased length of growing season, or other time dependent change in environment. Our study demonstrates that complex interactions between the host, the pathogen and the environment influence disease virulence of environmentally growing opportunistic pathogen.