Host phenology is an important driver of parasite transmission and evolution. In a seasonal environment, monocyclic, obligate-killer parasites evolve optimal virulence strategies such that all parasite progeny are released near the end of the host season to limit parasite progeny death in the environment. It is unclear whether host seasonality imposes different constraints on polycyclic parasites such that both polycyclic and monocyclic parasites are maintained. We develop a mathematical model of a disease system with seasonal host activity to study the evolutionary consequences of host phenology on polycyclic, obligate-killer parasite virulence strategies. Seasonal host activity patterns create both monocyclic and polycyclic parasite evolutionarily stable strategies (ESS) separated by less-fit strategies (evolutionary repellors). The ESS that evolves in each system is a function of the virulence strategy of the parasite introduced into the system. The trait value for both monocyclic and polycyclic strategies is determined by two aspects of host phenology: the duration of the host activity period and the distribution in the time at which hosts first become active within each season. Longer host activity periods and more synchronous host emergence drive both the monocyclic and polycyclic strategies towards lower virulence. The results demonstrate that host phenology can, in theory, maintain diverse parasite strategies among isolated geographic locations.