Grape phylloxera (Daktulosphaira vitifoliae Fitch) is a major global pest of cultivated grapevine. Armenia presents an unusual viticultural system, with 85-90% of vineyards remaining own-rooted despite the established presence of phylloxera. We investigated the genetic diversity and population structure of 370 root-feeding individuals collected from three localities in the Ararat Valley and Tavush Province using seven polymorphic simple sequence repeat markers. The seven loci yielded 48 alleles, with mean expected and observed heterozygosities of 0.570 and 0.933, re-spectively. Analysis of molecular variance revealed significant regional differentiation (Fst = 0.127, P = 0.001), driven primarily by differentiation between Tavush and the Ararat Valley popu-lations. The 370 individuals comprised 55 multilocus genotypes (MLGs), with two dominant MLGs represented by 171 and 116 individuals, together accounting for 77.6% of the sample. A population-aware, clone-corrected analysis of 59 MLG-by-population observations confirmed the same regional pattern and yielded stronger differentiation (Fst = 0.163, P = 0.001). Concordant separation of Tavush from the Ararat Valley was observed in principal coordinates analysis and discriminant analysis of principal components. The predominance of repeated MLGs is consistent with substantial clonal amplification. This study provides the first molecular baseline for D. vitifoliae in Armenia and establishes a foundation for monitoring genotype persistence, dispersal, and regional differentiation.