Understanding the genetics of host adaptation is a powerful approach to study host - parasite interactions. Hosts are often assumed to have a simple genetic architecture underlying resistance. However, in natural populations the genetics are rarely known and the link between host adaptation and evolutionary models cannot be easily established. To shed light on the genetic basis of host evolution in the presence and absence of parasites we studied a highly dynamic rockpool metapopulation of the planktonic crustacean Daphnia magna and its microsporidian parasite Hamiltosporidium tvaerminnensis. We examined genome-wide allele frequencies estimated from pooled Illumina sequencing (Pool-seq) of 12 subpopulations of a metapopulation. Subpopulations that had evolved for several years with the parasite were contrasted to uninfected subpopulations, with the aim to find genomic sites of diversifying selection. Consistent with earlier attempts to find resistance genes in this system, we observe many minor-effect outliers, suggesting that the response of the host to this parasite is based on a quantitative-trait architecture. We found 34 outliers across 11 genomic regions that indicate increased differentiation between population groups as well as signs of positive selection. Some of these regions contain immune-related genes, of which four are likely involved in immune downregulation. Our findings show that in the presence of the microsporidium parasite, hosts evolve in a complex polygenic way, driving population divergence in the metapopulation under study. Such evolutionary divergence is a powerful mechanism to maintain genetic diversity in spatially structured populations.