Fewer than half of the 80–100 North American species in parasitoid genus Coptera Say (Hymenoptera: Diapriidae) have been described. Hosts are known for just nine of these. The taxonomy of Coptera has been complicated by its cryptic morphology and a life history that includes parasitism of pupae beneath the surface of soils. Here, we describe collections targeting the host genus with which Coptera have most frequently been associated: flies in genus Rhagoletis (Loew) (Diptera: Tephritidae). DNA barcodes, morphology, and ecology (host associations) were used to understand species limits for Coptera collected from Rhagoletis. Four species of Coptera were recovered from five species of Rhagoletis, including a new species: Coptera n. sp. 1. Two of the associations with particular species of Rhagoletis were previously unknown, and no two species of Coptera were found to be attacking the same host, suggesting these four Coptera are specialist parasites. As several of the 25 North American species of Rhagoletis are agricultural pests, a better understanding of their natural associations with Coptera may prove valuable to biological control efforts.