Captorhinids are inherently interesting Paleozoic reptiles because they include the first terrestrial vertebrates to have multiple tooth rows on the maxilla and dentary. This may have been a key innovation that allowed captorhinids to diversify and disperse throughout the Permian Period of Pangea. We provide the first comparison of tooth development in captorhinids to determine how multiple rows of marginal teeth evolved within this clade. By comparing thin sections of multiple-rowed Captorhinus aguti from the Lower Permian of Oklahoma with the contemporaneous, single-rowed Captorhinus magnus, we provide evidence for variation in jaw growth, which establishes the number of tooth rows. Comparisons with the basal captorhinid Concordia cunninghami from the Upper Carboniferous of Kansas demonstrate that early captorhinids retained the typical amniote condition of replacing teeth in a manner similar to modern iguanian lizards. By comparing tooth development in C. aguti with other single-rowed captorhinids, we also demonstrate that the shedding of old teeth and the development of new teeth are not linked developmental processes in captorhinids. Instead, the fates of older generations of teeth are entirely dependent on their proximity to the lingual surface of the dentary where the toothproducing organ, the dental lamina, would have been present. These peculiar features of the dentitions of captorhinids make them model taxa for examining patterns of tooth development and replacement.