Experimental evolution can be used to test for and characterize parasite and pathogen adaptation. We undertook a serial-passage experiment in which a single parasite population of the obligate fungal (chytrid) parasite Rhizophydium megarrhizum was maintained over a period of 200 days under different mono- and multiclonal compositions of its phytoplankton host, the bloom-forming cyanobacterium Planktothrix. Despite initially inferior performance, parasite populations under sustained exposure to novel monoclonal hosts experienced rapid fitness increases evidenced by increased transmission rates. This demonstrates rapid adaptation of chytrids to novel hosts and highlights their high evolutionary potential. In contrast, increased fitness was not detected in parasites exposed to multiclonal host mixtures, indicating that cyanobacterial intraspecific diversity hampers parasites adaptation. Significant increases in intensity of infection were observed in monoclonal and multiclonal treatments, suggesting high evolvability of traits involved in parasite attachment onto hosts (i.e., encystment). A comparison of the performance of evolved and unevolved (control) parasite populations against their common ancestral host did not reveal parasite attenuation. Our results exemplify the ability of chytrid parasites to adapt rapidly to new hosts, while providing experimental evidence that genetic diversity in host populations grants increased resistance to disease by hindering parasite adaptation.