How large numbers of genes were recruited simultaneously to build new organ structures is one of the greatest puzzles in evolutionary biology. Here, we present data suggesting that the vegetative and reproductive classes of actins and other cytoskeletal proteins arose concurrently with the macroevolutionary divergence of leaves and reproductive structures in the earliest land plants. That the cytoskeleton is essential for physically programming the development of organs and tissues is well established. Thus, we propose that this regulatory dichotomy represents an ancient landmark event in the global regulation of hundreds of higher-plant genes, an event that is linked to the macroevolution of plant vegetative and reproductive organs. The recent availability of sequence and expression data for large numbers of plant genes should make it possible to dissect this and other major macroevolutionary events.