Ophiuroid systematics is currently in a state of upheaval, with recent molecular estimates fundamentally clashing with traditional, morphology-based classifications. Here, we attempt a long overdue recast of a morphological phylogeny estimate of the Ophiuroidea taking into account latest insights on microstructural features of the arm skeleton. Our final estimate is based on a total of 45 ingroup taxa, including 41 recent species covering the full range of extant ophiuroid higher taxon diversity and 4 fossil species known from exceptionally preserved material, and the Lower Carboniferous Aganaster gregarius as the outgroup. A total of 130 characters were scored directly on specimens. The tree resulting from the Bayesian inference analysis of the full data matrix is reasonably well resolved and well supported, and refutes all previous classifications, with most traditional families discredited as poly- or paraphyletic. In contrast, our tree agrees remarkably well with the latest molecular estimate, thus paving the way towards an integrated new classification of the Ophiuroidea. Among the characters which were qualitatively found to accord best with our tree topology, we selected a list of potential synapomorphies for future formal clade definitions. Furthermore, an analysis with 13 of the ingroup taxa reduced to the lateral arm plate characters produced a tree which was essentially similar to the full dataset tree. This suggests that dissociated lateral arm plates can be analysed in combination with fully known taxa and thus effectively unlocks the extensive record of fossil lateral arm plates for phylogenetic estimates. Finally, the age and position within our tree implies that the ophiuroid crown-group had started to diversify by the Early Triassic.