Although phosphate is an essential macronutrient for marine biota, critical to our understanding of marine productivity, biogeochemistry, and evolution, its long-timescale geologic history is poorly constrained. We constrain weathering-derived fluxes and seawater concentrations of phosphate throughout the Phanerozoic (541 Ma to present), by developing a model for the coupled, long-term biogeochemical cycles of phosphate, carbon, oxygen, and calcium. We find that the relative contribution of continental and seafloor weathering to the total weathering rate exerts a first-order control on ocean productivity, through a previously uninvestigated mechanism. Specifically, continental weathering is a source of the limiting nutrient phosphate, but seafloor weathering is not. As a result, times in Earth history in which seafloor weathering constitutes a large fraction of the total weathering rate (e.g., the early Paleozoic and Mesozoic), are also times in which phosphate delivery to the ocean is relatively low. A lower concentration of phosphate in seawater likely affected primary productivity, oceanic and atmospheric oxygen concentrations, with possible implications for the evolution of marine fauna over Earth history.