The abrupt origin and rapid diversification of the flowering plants during the Cretaceous has long been considered an “abominable mystery.” While the cause of their high diversity has been attributed largely to coevolution with pollinators and herbivores, their ability to outcompete the previously dominant ferns and gymnosperms has been the subject of many hypotheses. Common among these is that the angiosperms alone developed leaves with smaller, more numerous stomata and more highly branching venation networks that enable higher rates of transpiration, photosynthesis, and growth. Yet, how angiosperms pack their leaves with smaller, more abundant stomata and more veins is unknown but linked—we show—to simple biophysical constraints on cell size. Only angiosperm lineages underwent rapid genome downsizing during the early Cretaceous period, which facilitated the reductions in cell size necessary to pack more veins and stomata into their leaves, effectively bringing actual primary productivity closer to its maximum potential. Thus, the angiosperms’ heightened competitive abilities are due in no small part to genome downsizing.