Developmental gene regulatory networks (dGRNs) are assemblages of interacting regulatory factors that direct ontogeny of animal body plans. The hierarchical topology of these networks predicts that their nodes will evolve at different rates and consequently will bias the trajectories of embryonic evolution. To test this, detailed, comparative analyses of dGRNs that specify early, global embryonic domains are required. The most extensively detailed dGRNs have been documented for one of the two subclasses of extant sea urchins, the euechinoids. Remarkably, euechinoid dGRNs operating in early development show little appreciable change even though they diverged approximately 90 million years ago (mya). Therefore, to better understand the evolutionary dynamics of dGRNs, comparative microdissection must be undertaken for sea urchins that diverged deeper in geological time. Recent studies of cidaroids, the sister clade of euechinoid sea urchins, suggest that comparative analyses of their embryonic domain specification may prove insightful for understanding the evolutionary dynamics of dGRNs. Here, I report the spatiotemporal dynamics of 19 regulatory factors involved in dorsal-ventral patterning of non-skeletogenic mesodermal and ectodermal domains in the early development of Eucidaris tribuloides, a cidaroid sea urchin. Multiple lines of evidence indicate that deployment of ectodermal regulatory factors is more impervious to change than mesodermal regulatory factors in the sea urchin lineage and are supported by multiple lines of experimental evidence. Additionally, endogenous spatiotemporal expression data, intra-class reporter microinjections, and perturbation analyses of Nodal and Notch signaling allow the enumeration of numerous alterations to regulatory factor deployment since the divergence of echinoids. These results provide a global view of early embryonic developmental processes in two clades that diverged at least 268.8 mya and show that the dGRNs controlling embryonic specification exhibit differential lability, supporting the hypothesis that the topologies of dGRNs bias rates of evolutionary change and alter the developmental evolutionary trajectories of embryogenesis.