Risks of post-introduction evolution in insects introduced to control invasive pests have been discussed for some time, but little is known about responses to selection or genetic architectures of host adaptation and thus about the likelihood or rapidity of evolutionary shifts. We report here results on the response to selection and genetic architecture of parasitism of a sub-optimal, low-preference host species by an aphid parasitoid, Aphelinus rhamni, a candidate for introduction against the soybean aphid, Aphis glycines. The parasitoid was collected in Beijing, China, from the soybean aphid on a Rhamnus species. In the laboratory at the USDA-ARS, Newark, Delaware, we selected A. rhamni for increased parasitism of Rhopalsiphum padi by rearing the parasitoid on this aphid for three generations. We measured parasitism of R. padi at generations two and three, and at generation three, crossed and backcrossed parasitoids from the populations reared on R. padi with those from populations reared on Aphis glycines and compared parasitism of both R. padi and Aphis glycines among F1 and backcross females. Aphelinus rhamni responded rapidly to selection for parasitism of R. padi. Selection for R. padi parasitism reduced parasitism of Aphis glycines, the original host of A. rhamni. However, parasitism of R. padi did not increase from generation two to generation three of selection, suggesting reduced variance available for selection, which was indeed found. We tested the associations between 184 single nucleotide polymorphisms (SNP) and increased parasitism of R. padi and found 28 SNP loci, some of which were associated with increased and others with decreased parasitism of R. padi. We assembled and annotated the A. rhamni genome, mapped all SNP loci to contigs, and tested whether genes on contigs with SNP loci associated with parasitism were enriched for candidate genes or gene functions. We identified 80 genes on these contigs that mapped to 1.2 Mb of the 483 Mb genome of A. rhamni but found little enrichment of candidate genes or gene functions.