Schizaphis graminum Rondani (Hemiptera: Aphididae) and Sipha flava Forbes (Hemiptera: Aphididae) are two common pests of bioenergy grasses. Despite the fact that they are both considered generalists, they differ in their ability to colonize Panicum virgatum cultivars. For example, S. flava colonizes both P. virgatum cv. Summer and P. virgatum cv. Kanlow whereas S. graminum can only colonize Summer. To study the molecular responses of these aphids to these two switchgrass cultivars, we generated de novo transcriptome assemblies and compared the expression profiles of aphids feeding on both cultivars to profiles associated with feeding on a highly susceptible sorghum host and a starvation treatment. Transcriptome assemblies yielded 8,428 and 8,866 high-quality unigenes for S. graminum and S. flava, respectively. Overall, S. graminum responded strongly to all three treatments after 12 h with an upregulation of unigenes coding for detoxification enzymes while major transcriptional changes were not observed in S. flava until 24 h. Additionally, while the two aphids responded to the switchgrass feeding treatment by downregulating unigenes linked to growth and development, their responses to Summer and Kanlow diverged significantly. Schizaphis graminum upregulated more unigenes coding for stress-responsive enzymes in the Summer treatment compared to S. flava; however, many of these unigenes were actually downregulated in the Kanlow treatment. In contrast, S. flava appeared capable of overcoming host defenses by upregulating a larger number of unigenes coding for detoxification enzymes in the Kanlow treatment. Overall, these findings are consistent with previous studies on the interactions of these two cereal aphids to divergent switchgrass hosts.