Phosphorus is a critical nutrient controlling phytoplankton growth. Availability of this limiting factor can vary significantly in space and time, particularly in dynamic aquatic ecosystems. Diatoms are important eukaryotic phytoplankton that thrive in regions of pulsed phosphate supply, yet little is known of the sensory mechanisms enabling them to detect and rapidly respond to phosphorus availability. Here we show that phosphorus-starved diatoms utilise a novel Ca2+-dependent signalling pathway to sense and regulate cellular recovery following phosphorus resupply. This pathway, which has not previously been described in eukaryotes, is sensitive to sub-micromolar concentrations of phosphate, alongside a range of environmentally relevant phosphorus forms. Using comparative proteomics, we have characterised early adaptations governing diatom cellular recovery from phosphorus limitation. Strikingly, the dominant response was substantial enhancement of nitrogen assimilation proteins. This led to 12-fold increases in absolute nitrate uptake rates, relative to phosphorus-starved cells. Moreover, we find that the novel phosphorus-Ca2+ signalling pathway controls this primary recovery response. Our findings highlight that fundamental cross-talk between the essential nutrients phosphorus and nitrogen drive diatom recovery from phosphorus limitation. Moreover, a novel Ca2+-dependent phosphorus signalling pathway governs such ecological acclimation responses, and is thus likely critical to the success of diatoms in regions of episodic nutrient supply.