The receptor kinase FERONIA (FER) is a susceptibility factor for biotrophic powdery mildew fungal pathogens in Arabidopsis thaliana, but the underlying molecular mechanisms remain largely unknown. FER is required for the perception of endogenous RAPID ALKALINIZATION FACTOR (RALF) peptides to control various aspects of plant growth, development and immunity. RALFs are perceived by FER-LORELEI-LIKE GPI-ANCHORED PROTEIN (LLG) heterocomplexes to induce cellular responses and bind to LEUCINE-RICH REPEAT EXTENSIN (LRX) proteins as structural components of the cell wall. We show that FER`s RALF ligands are necessary for full success of powdery mildew colonization. Our data reveals that LLGs and LRXs are also powdery mildew susceptibility factors, and that the susceptibility function of RALFs is best explained by a combination of peptide signalling and cell wall-related effects. We further reveal that cell wall and apoplastic pH homeostasis, hallmark features of RALF function, support powdery mildew reproductive success. The function of host RALF peptides is underlined by the fact that, in contrast to previously described pathogens that hijack FER for colonization, powdery mildew fungi do not produce functional RALF mimics. Surprisingly, RALF-dependent powdery mildew pathogenesis is partially independent of FER. The resistance phenotype of ralf and fer mutants is not associated with de-regulated salicylic acid and jasmonic acid signalling, important defense-related phytohormones. Collectively, powdery mildew fungi require RALF signalling for apoplastic pH regulation and cell wall structural organization for successful colonization, highlighting a novel mechanism for host susceptibility by obligate biotrophic fungi.