The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today—demersal durophages all—these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals’ functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans’ distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.