Even though parasitic infections are often costly or deadly for the host, we know very little which genes influence parasite susceptibility and disease severity. Proliferative kidney disease (PKD) is an emerging and, at elevated water temperatures, potentially deadly disease of salmonid fishes that is caused by the myxozoan parasite Tetracapsuloides bryosalmonae. By screening > 7.6 K SNPs in 255 wild brown trout (Salmo trutta) and combining association mapping and random forest approaches, we identified several candidate genes for both the parasite resistance (inverse of relative parasite load; RPL) and the severe anemic response to the parasite. The strongest RPL-associated SNP mapped to a noncoding region of the congeneric Atlantic salmon (S. salar) chromosome 10, whereas the second strongest RPL-associated SNP mapped to an intronic region of PRICKLE2 gene, which is a part of the planar cell polarity signaling pathway involved in kidney development. The top SNP associated with anemia mapped to the intron of the putative PRKAG2 gene. The human ortholog of this gene has been associated with hematocrit and other blood-related traits, making it a prime candidate influencing parasite-triggered anemia in brown trout. Our findings demonstrate the power of association mapping to pinpoint genomic regions and potential causative genes underlying climate change-driven parasitic disease resistance and severity. Furthermore, this work illustrates the first steps towards dissecting genotype-phenotype links in a wild fish population using closely related genome information.