Gall wasps (Hymenoptera: Cynipidae) have fascinated researchers for centuries due to the elaborate diversity of charismatic galls they produce, the presence of unique reproductive systems (e.g., a form of cyclical parthenogenesis), the possible convergent evolution of semiparasitic gall wasp forms (i.e., “inquilines”), and their multitrophic interactions. While many classifications for gall wasps have been proposed, recent DNA sequence efforts combined with taxonomic revisions are beginning to clarify the evolutionary relationships of this group. To date, however, a well resolved phylogeny is lacking, complicating the study of outbreak-causing pest species. Outbreaks by one such species, the black oak gall wasp, Zapatella davisae Buffington & Melika (Hymenoptera: Cynipidae: Cynipini), have led to extensive damage and mortality of black oaks, Quercus velutina L. (Fagales: Fagaceae), in the northeastern United States. Here we sequenced fragments of the nuclear ribosomal gene 28S, and the nuclear protein coding gene long-wavelength opsin from samples of Z. davisae collected on Cape Cod, MA, and Long Island, NY. Using these sequences and sequences previously published from the mitochondrial locus cytochrome b, we performed Bayesian and maximum likelihood multilocus phylogenetic reconstructions based on a concatenated alignment including species of gall wasps in the tribe Cynipini from which all three loci were present in the GenBank database. Confirming morphological work, we find that Z. davisae is most closely related to species in the genera Callirhytis and Neuroterus, and appears to be a basal member of the “Quercus” section of the tribe Cynipini. We find that recent generic reclassifications within the Cynipini have made great progress towards clarifying the taxonomic relationships of species of gall-inducing wasps in this tribe, and we comment on several classifications that require additional research.