Unicellular, planktonic, prokaryotic and eukaryotic photoautotrophs (phytoplankton) have an ancient evolutionary history on Earth during which time they have played key roles in the regulation of marine food webs, biogeochemical cycles, and Earth's climate. Since they represent the basis of aquatic ecosystems, the manner in which phytoplankton die critically determines the flow and fate of photosynthetically fixed organic matter (and associated elements), ultimately constraining nutrient flow. Programmed cell death (PCD) and associated pathway genes, which are triggered by a variety of abiotic (nutrient, light, osmotic) and biotic (virus infection, allelopathy) environmental stresses, have an integral grip on cell fate, and have shaped the ecological success and evolutionary trajectory of diverse phytoplankton lineages. A combination of physiological, biochemical, and genetic techniques in model algal systems has demonstrated a conserved molecular and mechanistic framework of stress surveillance, signaling, and death activation pathways, involving collective and coordinated participation of organelles, redox enzymes, metabolites, and caspase-like proteases. This mechanistic understanding has provided insight into the integration of sensing and transduction of stress signals into cellular responses, and the mechanistic interfaces between PCD, cell stress and virus infection pathways. It has also provided insight into the evolution of PCD in unicellular photoautotrophs, the impact of PCD on the fate of natural phytoplankton assemblages and its role in aquatic biogeochemical cycles.