Fungicides are applied intensively to prevent downy mildew infections of grapevines (Vitis vinifera) with high impact on the environment. In order to develop alternative strategies we sequenced the genome of the oomycete pathogen Plasmopara viticola causing this disease. We show that it derives from a Phytophthora-like ancestor that switched to obligate biotrophy by losing genes involved in nitrogen metabolism and γ-Aminobutyric acid catabolism. By combining multiple omics approaches we characterized the pathosystem and identified a RxLR effector that trigger an immune response in the wild species V. riparia. This effector is an ideal marker to screen novel grape resistant varieties. Our study reveals an unprecedented bidirectional noncoding RNA-based mechanism that, in one direction might be fundamental for P. viticola to proficiently infect its host, and in the other might reduce the effects of the infection on the plant.