Paleobiologists must propose a priori hypotheses of homology when conducting a phylogenetic analysis of extinct taxa. The distributions of such “primary” homologies among species are fundamental to phylogeny reconstruction because they reflect a prior belief in what constitutes comparable organismal elements and are the principal determinants of the outcome of phylogenetic analysis. Problems arise when fossil morphology presents seemingly equivocal hypotheses of homology, herein referred to as antinomies. In groups where homology recognition has been elusive, such as echinoderms, these problems are commonly accompanied by the presence (and persistence) of poor descriptive terminology in taxonomic literature that confounds an understanding of characters and stymy phylogenetic research. This paper combines fossil morphology, phylogenetic systematics, and insights from evolutionary developmental biology to outline a research program in Phylogenetic Paleo-ontogeny. A “paleo” ontogenetic approach to character analysis provides a logical basis for homology recognition and discerning patterns of character evolution in a phylogenetic context. To illustrate the utility of the paleo-ontogenetic approach, I present a reassessment of historically contentious plate homologies for “pan-cladid” crinoids (Cladida, Flexibilia, Articulata). Developmental patterns in living crinoids were combined with the fossil record of pan-cladid morphologies to investigate primary posterior plate homologies. Results suggest the sequence of morphologic transitions unfolding during the ontogeny of extant crinoids are developmental relics of their Paleozoic precursors. Developmental genetic modules controlling posterior plate development in pan-cladid crinoids have likely experienced considerable constraint for over 250 million years and limited morphologic diversity in the complexity of calyx characters. Future phylogenetic analyses of pan-cladids are recommended to consider the presence of a single plate in the posterior region homologous with the radianal, rather than the anal X, as is commonly assumed.