The origins and maintenance of morphological diversity through the Phanerozoic have been documented in several groups of invertebrates. By using shape analysis of the ventral valve, we quantify morphological diversity within the inarticulate brachiopods, which have a species-rich lower Paleozoic history followed by low richness through the rest of the Phanerozoic. Morphological diversity peaked during the Cambrian, and was subsequently maintained despite significant decreases in richness at all taxonomic levels. The loss of morphological diversity, associated with late-Paleozoic decreases in the number of orders and the Permo-Triassic mass extinction, was followed by rapid morphological rediversification without concordant taxonomic diversification. Any limits upon the generation of diverse morphologies were established early in the Cambrian and were maintained and approached through the history of this group.