Kelps are key primary producers of cold and temperate marine coastal ecosystems and exhibit systemic defences against pathogens. Yet, the cellular mechanisms underpinning their immunity remain to be elucidated. We investigated the time course of infection of the kelp Macrocystis pyrifera by the oomycete Anisolpidium ectocarpii using TEM, in vivo autophagy markers, and autophagy inhibitors. Over several infection cycles, A. ectocarpii undergoes sequential physiological shifts sensitive to autophagy inhibitors. Initially lipid-rich, pathogen thalli become increasingly lipid-depleted; they subsequently tend to become entirely abortive, irrespective of their lipid content. Moreover, infected algal cells mount local defences and can directly eliminate the pathogen by xenophagy. Finally, autophagy-dependent plastid recycling is induced in uninfected host cells. We demonstrate the existence of local, inducible autophagic processes both in the pathogen and infected host cells, which result in the restriction of pathogen propagation. We also show the existence of a systemic algal response mediated by autophagy. We propose a working model accounting for all our observations, whereby the outcome of the algal-pathogen interaction (i.e. completion or not of the pathogen life cycle) is dictated by the induction, and possibly the mutual hijacking, of the host and pathogen autophagy machineries.