Oat (Avena sativa L.) is a widely cultivated cereal crop valued for both its nutritional benefits and agricultural versatility. However, oat production is increasingly challenged by powdery mildew, which is caused by Blumeria graminis f. sp. avenae (Bga) and can lead to considerable yield losses. Genetic resistance remains the most sustainable and environmentally friendly method of disease control. This study aimed to evaluate the effectiveness of 14 oat genotypes carrying known resistance genes (Pm1–Pm12) and Avena strigosa accessions against Bga populations collected across four regions of Poland between 2021 and 2023. Host–pathogen assays were used to assess resistance levels, virulence frequency, and pathotype diversity. Resistance genes were categorized into three groups based on performance: highly effective (Pm2, Pm4, Pm5, Pm7 in APR122 and A. strigosa), variably effective (Pm7 in ‘Canyon’ and Pm9–Pm12), and moderately effective (Pm1, Pm3, Pm6 and Pm3+8). Pathogen populations exhibited decreasing virulence complexity and diversity over time, with substantial regional variation. There were few dominant pathotypes, but most were rare and transient. This study confirms the long-term effectiveness of several resistance genes and the necessity of continuous resistance monitoring. It supports the use of gene pyramiding to ensure durable, regionally adapted protection. These results highlight the importance of combining resistance breeding with integrated disease management to ensure sustainable oat production under changing environmental conditions.