The exact affinities of the fossil teeth attributed to the devilrays (mobulids) are critical for resolving the debated origin of these giant pelagic rays amongst Myliobatiformes and the timing of their evolution toward planktivory. We performed the first detailed comparative description of teeth belonging to most of the living and fossil mobulids. Based on a survey of living devilrays, three dental morphologies are newly identified as cobblestone tooth plates, comb-like teeth, and peg-like teeth. In addition, all extinct mobulid species are reviewed with comments on their dentition, fossil record, and geographical distribution. As a result, three fossil mobulid taxa are newly described from the Late Eocene of south-west Morocco (Argoubia barbei gen. et sp. nov., Oromobula dakhlaensis gen. et sp. nov., and Eoplinthicus underwoodi sp. nov.). This has permitted the first assessment of the phylogenetic positions of extinct and extant species of mobulids, using cladistic analyses and a combined data set of nondental anatomical characters from the literature and the dental characters defined here. Our new results support the monophyly of mobulids including all living and most extinct species and indicate that mobulids are closely related to rhinopterids. They also indicate that there was a recent split within Mobulidae into the three tooth morphology groups that we describe in this paper. This work provides clues to the evolutionary history of this clade since the Early Eocene, including the gradual lack in tooth interlocking toward the filter-feeding strategy, whereas the preservation of cusped teeth without feeding function in modern filter-feeder mobulids is interpreted as a tool for precopulatory purposes.