<p>Oak powdery mildew, caused by <i>Erysiphe alphitoides</i>, is a widespread disease that affects oaks. We aimed to understand the complex interactions between extrinsic (environmental) and intrinsic (provenance) factors that influence the infection rate of <i>E. alphitoides</i> on <i>Quercus robur</i> seedlings. In a common garden controlled water experiment, we investigated the natural infection rate of <i>E. alphitoides</i> considering factors such as oak provenance, soil moisture availability, and the seedlings’ location in the microenvironment. We examined infection rates on first- and second-flush leaves, assessed oak gas exchange responses (net photosynthesis, transpiration, and stomatal conductance) to powdery mildew infections, and evaluated stomatal size and density as a potential pathway for pathogen entry. Our results showed that different factors influence first and second-flush leaf infection rates. First flush infections were milder, primarily depending on provenance (an intrinsic factor), with early leaf development correlating with lower infection rates. Second flush leaf infections in summer were more severe, driven by extrinsic factors such as the microenvironment and water availability, with spore dispersal influenced by prevailing wind direction. We observed a significant effect of <i>E. alphitoides</i> on photosynthesis, along with reduction in infection rates under drought. This suggests that stomatal closure—reflected in reduced stomatal conductance—under drought stress may prevent pathogen penetration. Moreover, our results suggest that stomatal closure itself, rather than the size of the stomatal pore, may play a more critical role in limiting pathogen entry. Further assessment of biochemical defenses in drought-stressed seedlings could help clarify if additional mechanisms are involved.</p>