Abstract DNA demethylase (DML) is involved in plant development and responses to biotic and abiotic stresses; however, its role in plant–herbivore interaction remains elusive. Here, we found that herbivory by the potato tuber moth, Phthorimaea operculella, rapidly induced the genome-wide DNA methylation and accumulation of DML gene transcripts in potato plants. Herbivory induction of DML transcripts was suppressed in jasmonate-deficient plants, whereas exogenous application of methyl jasmonate (MeJA) improved DML transcripts, indicating that the induction of DML transcripts by herbivory is associated with jasmonate signaling. Moreover, P. operculella larvae grew heavier on DML gene (StDML2) knockdown plants than on wild-type plants, and the decreased biosynthesis of jasmonates in the former may be responsible for this difference, since the larvae feeding on these two genotypes supplemented with MeJA showed similar growth. In addition, P. operculella adult moths preferred to oviposit on StDML2 knockdown plants than on wild-type plants, which was associated with the reduced emission of β-caryophyllene in the former. In addition, supplementing β-caryophyllene to these two genotypes further disrupted moths’ oviposit choice preference for them. Interestingly, in StDML2 knockdown plants, hypermethylation was found at the promoter regions for the key genes StAOS and StAOC in the jasmonate biosynthetic pathway, as well as for the key gene StTPS12 in β-caryophyllene production. Our findings suggest that knocking down StDML2 can affect herbivore defense via jasmonate signaling and defense compound production in potato plants.