Organisms from the five kingdoms of life use minerals to from hard structures that protect and support them, in the process of biomineralization. The ability of cells to control mineral phase, growth and shape, is beyond the state-of-the-art of human technologies and fascinated scientists. Little is known about the molecular mechanisms that control localized biomineral deposition, growth and shape. The sea urchin larval skeletogenesis provides an excellent system to study the molecular control of biomineralization. The sea urchin skeletogenic gene regulatory network is known in great details and assumingly evolved from an ancestral tubulogenesis program from which vertebrates’ vascularization had evolved. During vertebrates’ vascularization, VEGF signaling activates Rho-associated coiled-coiled containing kinase (ROCK), that is crucial for blood vessel formation. Here we reveal that during sea urchin skeletogenesis, VEGF signaling drives ROCK activity which is essential for skeleton formation, skeletal elongation and normal branching. ROCK controls the accumulation of actin filaments around the forming calcite spicules. As the spicule elongates, actin filaments and key skeletogenic genes are enriched at the tips of the skeletal rods, the place where rapid growth occurs. Under ROCK inhibition, the tip-specific regulatory and actomyosin state, lingers behind and expands to the multiple ectopic tips that form. Our studies suggest that actomyosin remodeling controls localized mineral deposition, growth, and skeletogenic gene expression. We propose that cytoskeleton remodeling is a common driver of biomineralization that controls the growth and shape of the forming biomineral.