Gene transfer among reproductively isolated organisms can lead to novel phenotypes and increased fitness. Among the Sternorrhyncha, a suborder of plant sap-feeding hemipteran insects, both aphids and adelgids acquired carotenoid biosynthesis genes from a fungal donor that result in ecologically relevant pigmentation. Phylloxerids form another family that are closely related to aphids and adelgids and share similar pigmentation, but are largely uncharacterized for their presence and number of pigment genes that have duplicated among aphids. Here, we examined the transcriptomes of nine phylloxerid species, and performed PCR to amplify carotenoid genes from their genomic DNA. We identified carotenoid cyclase/synthase and desaturase genes in each species and demonstrated that they share the common fungal origin as those of aphids and adelgids based on their exon-intron gene structures and phylogenetic relationships. The phylogenetic analyses also indicated that carotenoid genes evolved following the differentiation of aphids, adelgids, and phylloxerids at the levels of family, genus, and species. Unlike aphids that duplicated these genes in their genomes, phylloxerids maintained only single copies, and some species may lack expression of certain genes. These results suggest that the phylloxerid lifestyle undergoes reduced selection pressure to expand carotenoid synthesis genes, and provides insight into these gene functions in insects.