The parasitoid wasp, Hyposoter horticola, parasitizes a nearly fixed fraction of its host butterfly larvae within a host metapopulation of 300-500 local populations in a 50 x 70-km area. We show, through laboratory observation, that the wasp lays eggs in fully developed larvae that have not yet hatched from the egg, constraining the period of host vulnerability to several hours out of the host's one year lifecycle. The parasitoid achieves a persistent high rate of parasitism over the entire host range despite the extremely limited period of host vulnerability as well as a high rate of host population extinctions and colonizations of new habitat patches every year. It does this in part by being extremely mobile. In addition, we show by using a field experiment and observation of marked wasps foraging for hosts in natural populations, that the wasp finds virtually all host egg clusters in the weeks before the hosts become vulnerable to parasitism, and then later returns to parasitize them. By locating the hosts before their vulnerability, the wasp extends the time available for searching from hours to weeks. After parasitizing about one-third of the larvae in a host cluster the wasp stops, apparently leaving a mark that deters further parasitism by other individuals. The result of this novel combination of mobility and local foraging behavior is a stable population size despite an unstable host that is vulnerable during about one thousandth of its lifecycle. Reproduction; Reproductive behaviour; Parasites diseases and disorders; Parasites; Insect parasites; Hosts; Insect hosts; Ecology; Land zones; Palaearctic region; Eurasia; Europe Melitaea cinxia (Nymphalidae); Hymenopteran parasites; Hyposoter horticola; Parasite behaviour related to host availability; Population dynamics; Finland; Southwest; Aland Islands; Hymenopteran parasite behaviour related to host availability Hyposoter horticola (Ichneumonidae); Egg laying; Lepidopteran hosts; Melitaea cinxia; Parasite behaviour related to host availability; Finland; Southwest; Aland Islands; Female behaviour related to lepidopteran host availability none