Phosphate is an essential macronutrient for all organisms with a key role in setting levels of marine primary productivity. Despite its importance for marine biogeochemical cycles and its role in shaping the evolution of marine organisms, the factors controlling phosphate bioavailability on geologic timescales remain poorly understood. Here we develop a statistical model of the coupled cycles of phosphate, carbon, oxygen and calcium to constrain the weathering-derived fluxes and seawater concentrations of phosphate through Phanerozoic time (541 million years ago to the present). Our model includes input parameters and time-dependent forcings derived from geologic and geochemical data. We find that the climate sensitivity of chemical weathering of the oceanic crust by low-temperature fluids exerts a first-order control on phosphate availability. Specifically, continental weathering is a source of the limiting nutrient phosphate, but seafloor weathering is considered to be a minor phosphate sink. Consequently, times in Earth history during which seafloor weathering constituted a large fraction of the total (seafloor + continental) weathering were also times during which phosphate influxes to and concentrations in the ocean were relatively low. Lower seawater phosphate levels during those times probably resulted in lower primary productivity and oceanic and atmospheric oxygen concentrations.