The activation of programmed cell death in the host during plant–pathogen interactions is an important component of the plant disease resistance mechanism. In this study we show that activation of programmed cell death in microorganisms also regulates plant–pathogen interactions. We found that a form of vacuolar cell death is induced in the oomycete Phytophthora parasitica– the agent that causes black shank disease in Nicotiana tabacum– by extracellular stimuli from resistant tobacco. The single-celled zoospores underwent cell death characterized by dynamic membrane rearrangements, cell shrinkage, formation of numerous large vacuoles in the cytoplasm and degradation of cytoplasmic components before plasma membrane disruption. Phytophthora cell death required protein synthesis but not caspase activation, and was associated with the production of intracellular reactive oxygen species. This characterization of plant-mediated cell death signalling in pathogens will enhance our understanding of the biological processes regulating plant–pathogen interactions, and improve our ability to control crop diseases.