Until recently, the foliar forms of grape phylloxera have been absent or very rare in California, and nodosities have not been common on resistant rootstocks. Foliar phylloxera are now widely spread in the mothervine plantings of grape rootstock nurseries in Yolo and Solano counties. Nodosities on resistant rootstocks have also been frequently observed. To determine the genetic relationships within and among these seemingly new types of phylloxera, collections were made across California from 2009 to 2011. Foliar-feeding phylloxera strains were collected from rootstock mothervines at the National Clonal Germplasm Repository in Winters, CA; University of California, Davis (UCD), vineyards; and six commercial rootstock nursery plantings in Yolo and Solano counties. Root-feeding samples were collected from a rootstock trial at the UCD Oakville research station vineyard in Napa County, which had previously been sampled in 2006 and 2007. Root-feeding samples were also collected from commercial vineyards in Napa and Sonoma counties and UCD vineyards. All samples were tested and genotyped using simple sequence repeat markers, and the genetic structure of the populations was analyzed. The results identified four genetically distinct populations of phylloxera in California, which were named Davis, Foliar, Napa1, and Napa2. Davis, Napa1, and Napa2 were composed of root-feeding samples. Multilocus genotypes with identical DNA-fingerprint profiles were detected in the 2006 to 2007 samples from the Oakville research station. More genetic divergence was observed in the Davis, Napa1, and Napa2 populations, with evidence for sexual reproduction between members of Napa1 and Napa2. The Foliar population consisted of only foliar-feeding samples with multilocus genotypes that were not detected prior to 2009; asexual reproduction was clearly the primary reproductive mode.