Close interactions between insects and plants have played a major role in the evolution of both these diverse groups of organisms. Studying these interactions, however, can be difficult because many insects, especially parasites, impinge most strongly on plants during larval stages when they are morphologically difficult to identify, and many belong to diverse groups for which most species remain undescribed. We used DNA barcoding to identify nondescript lepidopteran larvae that regularly parasitize flower buds of the coastal dune endemic Camissoniopsis cheiranthifolia (Onagraceae). We obtained cytochrome oxidase 1 mitochondrial DNA sequences from 201 parasite specimens from across the host geographical range. The Barcode of Life Database Identification System combined with Bayesian analysis grouped all 15 parasite haplotypes in a distinct, monophyletic clade within the genus Mompha (Lepidoptera: Coleophoridae: Momphinae), a group known to be host specialists on plants of the Onagraceae. Species identity and phylogenetic affinities within Mompha could not be confirmed because few barcode sequences exist from this diverse and poorly known group of moths. However, morphological analysis, including detailed dissection of genitalia for a subsample of 23 reared adults and comparison with known species of Mompha, also indicated that the larvae parasitizing C. cheiranthifolia constitute a distinct and undescribed species within this genus. Knowing that floral parasitism of C. cheiranthifolia involves a single, putatively host-specific microlepidopteran greatly facilitates formulating and testing hypotheses concerning how floral parasitism has promoted the evolution of striking floral diversity within this species. More generally, DNA barcoding combined with morphological analysis can greatly hasten identification of problematic specimens and enhance our understanding of the diversity, ecology and evolution of plant–insect interactions.