The extant megamouth shark, Megachasma pelagios (Lamniformes: Megachasmidae), is a large filter-feeding fish. We here describe a new species of Megachasma, M. applegatei, sp. nov., a putative sister species of the extant M. pelagios, based on isolated teeth from late Oligocene—early Miocene (late Chattian—Aquitanian) marine deposits in California and Oregon, U.S.A. Although showing a megachasmid tooth design, teeth of M. applegatei, sp. nov., exhibit a wide morphological range and are reminiscent to those of odontaspidid sharks with strong heterodonty. Megachasma applegatei, sp. nov., could have commonly measured approximately 6 m in total length and likely had a wide range of diet, possibly including small fishes and planktonic invertebrates. The fossil record indicates that either M. applegatei, sp. nov., was broadly adapted to a wide bathymetric tolerance or was a nektopelagic feeder over both deep and shallow water habitats.