Plant diseases are a major cause for yield losses and new strategies to control them without harming the environment are urgently needed. Plant-associated bacteria contribute to their host's health in diverse ways, among which the emission of disease-inhibiting volatile organic compounds (VOCs). We have previously reported that VOCs emitted by potato-associated bacteria caused strong in vitro growth inhibition of the late blight causing agent Phytophthora infestans. This work focuses on sulfur-containing VOCs (sVOCs) and demonstrates the high in planta protective potential of S-methyl methane thiosulfonate (MMTS), which fully prevented late blight disease in potato leaves and plantlets without phytotoxic effects, in contrast to other sVOCs. Short exposure times were sufficient to protect plants against infection. We further showed that MMTS's protective activity was not mediated by the plant immune system but lied in its anti-oomycete activity. Using quantitative proteomics, we determined that different sVOCs caused specific proteome changes in P. infestans, indicating perturbations in sulfur metabolism, protein translation and redox balance. This work brings new perspectives for plant protection against the devastating Irish Famine pathogen, while opening new research avenues on the role of sVOCs in the interaction between plants and their microbiome.