Our understanding of the origin, evolution, and biogeography of seafloor fauna is limited because we have insufficient spatial and temporal data to resolve underlying processes. The abundance and wide distribution of modern and disarticulated fossil Ophiuroidea, including brittle stars and basket stars, make them an ideal model system for global marine biogeography if we have the phylogenetic framework necessary to link extant and fossil morphology in an evolutionary context. Here we construct a phylogeny from a highly complete 425-gene, 61-taxa transcriptome-based data set covering 15 of the 18 ophiuroid families and representatives of all extant echinoderm classes. We calibrate our phylogeny with a series of novel fossil discoveries from the early Mesozoic. We confirm the traditional paleontological view that ophiuroids are sister to the asteroids and date the crown group Ophiuroidea to the mid-Permian (270 ± 30 mega-annum). We refute all historical classification schemes of the Ophiuroidea based on gross structural characters but find strong congruence with schemes based on lateral arm plate microstructure and the temporal appearance of various plate morphologies in the fossil record. The verification that these microfossils contain phylogenetically informative characters unlocks their potential to advance our understanding of marine biogeographical processes.