Epigenetic patterns including DNA methylation are known to vary between distantly related species, but it is not clear how these patterns differ at an intraspecific level. The sweetpotato whitefly, Bemisia tabaci (Gennadius) (Aleyrodidae; Hemiptera), encompasses several cryptic species. These cryptic species possess highly similar genomes but exhibit substantial biological and physiological differences. B. tabaci cryptic species are invasive, highly polyphagous, and transmit an array of plant infecting single stranded DNA viruses (ssDNA) –begomoviruses. In this study, DNA methylation patterns around genes and genomic features of two prominent B. tabaci cryptic species were investigated following acquisition of a monopartite ssDNA virus –tomato yellow curl virus. The cryptic species investigated included: B (also known as Middle East Asia Minor 1) and Q (also known as Mediterranean). Genomic features, such as promoters, gene bodies, and transposable elements were assessed for methylation levels in both B and Q cryptic species. Differentially methylated regions within predominantly unique genes were identified in B and Q cryptic species, respectively. All differentially methylated regions were assessed for differential gene expression and alternative splicing events with and without virus acquisition. The differentially expressed genes were further grouped into hyper- and hypomethylated clusters. These clusters included genes with implications for virus-vector interactions including immune functions and xenobiotics’ detoxification. The observed DNA methylation pattern differences within each cryptic species could, in part, explain some of the biological and physiological differences between them.