Novel trophic associations have sometimes resulted in fortuitous and significant biological control. After the invasion of North America by the South American cactus moth, Cactoblastis cactorum (Berg) (Pyralidae: Phycitinae), it is pertinent to characterize the assemblage of local natural enemies that could utilize this moth in new host-parasitoid associations. Herein we report on Apanteles mimoristae Muesebeck (Braconidae: Microgastrinae), a North American gregarious endoparasitoid wasp attacking the caterpillar of the phycitine cactus moth Melitara cf. nephelepasa (Dyar) (Pyralidae: Phycitinae, also known as zebra worm), also native to North America; both collected in Opuntia ficus-indica (L.) Mill. (Cactaceae) cultivated fields at rural areas of Mexico City. We provide an updated morphological account for A. mimoristae visualized with light microscopy and scanning electron microscope (SEM); a fragment of its cytochrome oxidase subunit I (COI) gene sequence data is reported for the first time. Additionally, we analyze its taxonomical position relative to other Apanteles species from the Americas including those attacking cactus-feeding moths. Our analyses place A. mimoristae (from Mexico) in a clade with A. esthercentenoae Fernández-Triana (from Costa Rica), a parasitoid of both Cromarcha stroudagnesia Solis (Pyralidae) and Palpita venatalis (Schaus) (Crambidae) (non cactus-feeding), and in a sister clade to A. opuntiarum Martínez & Berta (from Argentina) and A. alexanderi Brèthes (from Argentina and Uruguay), parasitoids of the cactus-feeding phycitines Cactoblastis and Tucumania respectively. Finally, we provide an updated key for the identification of Apanteles species recorded parasitizing cactus moth caterpillars in the American continent.