Embryonic development is a genomically encoded construction process in which cells acquire their identities and build organs within a three-dimensional embryonic environment. A central question in developmental biology is: once cells know who they are, how do they construct the organs they are set to form? We address this question by studying the relatively simple system of sea urchin skeletogenesis, focusing on the interplay between gene regulatory networks (GRNs) that specify cell identity and cytoskeletal and adhesion protein networks that drive cell behavior and morphogenesis. The sea urchin larval skeleton is composed of two calcite spicules, which grow within a tubular cavity formed by skeletogenic cells. Our recent findings suggest that the GRN governing this process evolved from an ancestral tubulogenesis program, which also gave rise to the GRN that drives blood vessel formation in vertebrates. As the spicules grow and stiffen, they trigger a cellular response involving adhesion and cytoskeletal remodeling proteins—regulating further skeletal growth and feeding back into the GRN itself. Strikingly, a similar regulatory circuit is active in vertebrate bone cells, suggesting it was independently co-opted in the evolution of biomineralization in both echinoderms and vertebrates in response to increased matrix stiffness. Together, our studies reveal how mechanical and genetic signals are integrated to guide organ formation and how these signals have been repurposed to support evolutionary innovation.