The obligate oomycete Pseudoperonospora cubensis causes cucurbit downy mildew (CDM) on a broad range of Cucurbitaceae host plants. Until 2004, CDM was managed primarily by host resistance in cucumber and modest fungicide applications in other cucurbits in the United States (US). However, since the 2004 epidemic, management relies on frequent fungicide applications, especially in cucumber where fungicide resistance has already been reported for several chemistries. Genetic analysis of pre- and post-epidemic samples revealed that P. cubensis is subdivided into two distinct clades with host specialization and differential response to certain fungicides. While Clade I was predominant among pre-2004 US P. cubensis samples, post-2004 samples exhibited a mix of Clade I and II. However, P. cubensis from international sources exhibited either Clade I or Clade II often from the same host plant. Using this information and comparative genomics approaches we developed a biosurveillance system for CDM that relies on spore traps and provides information about inoculum level, crop risk, and fungicide resistance for precision disease management within a growing season. Our findings not only provide insight into the causes of the 2004 CDM epidemic, but will significantly improve P. cubensis management by shifting current practices to crop specific recommendations for growers that account for population dynamics.