1. Theory predicts that organisms should invest in overcoming a factor that may limit their reproductive success in direct proportion to their probability of being limited by it. The occurrence of egg limitation (where female insects deplete their eggs while oviposition opportunities are still available) is predicted to impose selection for increased fecundity at the expense of other fitness components. 2. We tested the hypothesis that the fecundity of a proovigenic 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. 3. We studied the proovigenic 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. 4. We found that leafhopper density was higher at vineyards than in riparian habitats, whereas leafhopper egg size 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 lifespan. 5. 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. 6. The ability of parasitoid fecundity to track mean host availability may strengthen the ability of parasitoids to suppress the population densities of their hosts, and hence may represent an important ecological or eco-evolutionary feedback.