- Summary Theory predicts that organisms should invest more heavily in overcoming factors that more frequently emerge as the primary constraints to fitness, and especially, those factors that constrain the fitness of the most highly reproductive members of the population. We tested the hypothesis that the fecundity of a pro-ovigenic parasitoid (where females emerge with their full egg load) should be positively correlated with the mean expectation for oviposition opportunities in the environment. More specifically, we tested whether females from agricultural systems, where hosts are often relatively abundant, emerge with more eggs than those from natural habitats. We studied the pro-ovigenic parasitoid wasp Anagrus daanei, which parasitizes eggs of leafhoppers of the genus Erythroneura. Erythroneura spp. leafhoppers feed on Vitis spp. (grapes) and are major pests of commercial vineyards as well as common herbivores of wild Vitis californica, which grows in riparian habitats. We sampled leafhoppers and parasitoids from eight vineyards and eight riparian habitats in central California. We found that leafhopper density was higher at vineyards than in riparian habitats, whereas leafhopper egg volume and parasitoid body size did not differ among these habitat types. Parasitoids from vineyards had higher egg loads than parasitoids from wild grapes, and fecundity was positively related to host density across field sites. Parasitoid egg volume was larger in natural sites; however, this variation was not significantly correlated with host density across field sites. Within a single population of parasitoids collected from a vineyard, parasitoid egg load was negatively correlated with longevity, suggesting a trade-off between reproduction and life span. The results may be explained by a rapid evolution of reproductive traits in response to oviposition opportunities; or alternatively, by the occurrence of maternal effects on the fecundity of daughters based on the foraging experience of their mothers. The ability of parasitoid fecundity to track mean host availability is likely to modulate the likelihood that parasitoid fitness will be constrained by a shortage of eggs and strengthen the ability of parasitoids to suppress the population densities of their hosts.