Holocephalans (ratfish, rabbitfish and chimaeras) figure with increasing prominence in studies of gnathostome evolutionary biology. Here, we provide the first complete description of the teeth and toothplates of one of the earliest known holocephalans, Chondrenchelys problematica, including the first unambiguous evidence of a gnathostome with an extra-mandibular dentition. We further demonstrate that holocephalan toothplate ontogeny differs fundamentally from all other extant gnathostome examples, and show how the conjunction of these teeth and toothplates challenges the monophyly of an extinct chondrichthyan clade, the Petalodontiformes. Chondrenchelys provides a novel perspective on the evolution of dentitions in shark-like fishes, expands the known repertoire of gnathostome dental morphologies and offers a glimpse of radically new chondrichthyan ecomorphs, now lost from the modern biota, following the end-Devonian extinctions.