Parasite-switching to novel hosts has profound effects on ecological and evolutionary disease dynamics. Switching requires that parasites are able to establish contact with hosts and overcome host-defenses. Pathogenic fungal species in the genus Escovopsis, which attack and consume the fungi cultivated by fungus-growing ants, are attracted to their hosts via chemotaxis. This adaptation is host-specific; Escovopsis spp. grow toward their natural hosts more rapidly than toward other closely-related fungal cultivars and rarely are attracted to cultivars distantly related to their typical hosts. Moreover, cultivars secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific; cultivars cannot inhibit most isolates of their typical pathogens but often inhibit isolates of novel Escovopsis. Antibiotic defenses against Escovopsis provided by co-evolving actinomycete bacteria on the ants do not show the same patterns of specificity as those elicited by the host cultivars. Overall, complex chemotactic and antibiotic responses may explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host-parasite coevolution within the ancient fungus-growing ant-microbe association.