The diversity of parasitic insects remains one of the most conspicuous patterns on the planet. The principal factor thought to contribute to differentiation of populations and ultimately speciation is the intimate relationship parasites share with hosts and the potential for disruptive selection associated with using different host species. Traits that generate this diversity have been an intensely debated topic of central importance to the evolution of specialization and maintenance of ecological diversity. A fundamental hypothesis surrounding the evolution of specialization is that no single genotype is uniformly superior in all environments. This “trade-off” hypothesis suggests that negative fitness correlations can lead to specialization on different hosts as alternative stable strategies. In this study we demonstrate a trade-off in the ability of the parasitoid, Aphidius ervi, to maintain a high level of fitness on an ancestral and novel host, which suggests a genetic basis for host utilization that may limit host-range expansion in parasitoids. Furthermore, behavioral evidence suggests mechanisms that could promote specialization through induced host fidelity. Results are discussed in the context of host-affiliated ecological selection as a potential source driving diversification in parasitoid communities and the influence of host species heterogeneity on population differentiation and local adaptation.