A number of echinoderm species have replaced indirect development with highly modified direct-developmental modes, and provide models for the study of the evolution of early embryonic development. These divergent early ontogenies may differ significantly in life history, oogenesis, cleavage pattern, cell lineage, and timing of cell fate specification compared with those of indirect-developing species. No direct-developing echinoderm species has been studied at the level of molecular specification of embryonic axes. Here we report the first functional analysis of Wnt pathway components in Heliocidaris erythrogramma, a direct-developing sea urchin. We show by misexpression and dominant negative knockout construct expression that Wnt8 and TCF are functionally conserved in the generation of the primary (animal/vegetal) axis in two independently evolved direct-developing sea urchins. Thus, Wnt pathway signaling is an overall deeply conserved mechanism for axis formation that transcends radical changes to early developmental ontogenies. However, the timing of expression and linkages between Wnt8, TCF, and components of the PMC-specification pathway have changed. These changes correlate with the transition from an indirect- to a direct-developing larval life history.