In this dissertation, the integrated metabolism of three aphid species (Acyrthosiphon pisum, Aphis glycines, and Myzus persicae) and their specialized endosymbionts was explored. In the first chapter, tissue- and host plant-specific profiles of gene expression and CpG methylation of A. pisum were analyzed. Through RNA-Seq and whole genome bisulfite sequencing, I identified key metabolic genes that are differentially expressed and methylated between bacteriocytes and body cells. Moreover, I demonstrated for the first time that key aphid genes involved in the regulation of aphid-Buchnera symbiosis are differentially expressed and methylated depending on the aphid’s host plant diet, suggesting that DNA methylation may be a key regulatory factor that induces phenotypic variation depending on the host plant diet. In the second aphid system, I empirically and computationally confirmed the functional CpG methylation system in Aphis glycines. Also, I showed that lineage-specific genes in A. glycines have significantly lower CpG methylation levels compared to evolutionarily conserved genes. Moreover, five aphid-specific genes were identified to play key roles in insect-plant interactions at the epigenetic level. In the last aphid system, I identified differentially expressed genes in bacteriocytes of Myzus persicae compared to its body cells. I demonstrated overall up-regulation of the genes that are involved in amino acid biosynthesis as well as key genes in aphid-Buchnera integrated metabolism. I then compared gene expression patterns of M. persicae bacteriocytes to those of A. pisum bacteriocytes. I found that the two closely related species have very similar gene expression profiles in their bacteriocytes while there are lineage-specific expression signatures in some metabolic genes.