The plasmodiophoromycete Polymyxa betae is an obligate root parasite that transmits Beet necrotic yellow vein virus (BNYVV), the cause of sugar beet rhizomania disease. Currently, control of this disease is achieved through the use of cultivars with monogenic (Rz1) partial resistance to the virus. To improve the level and durability of this resistance, sources of resistance to the virus vector, P. betae, were sought. Over 100 accessions of the wild sea beet (Beta vulgaris ssp. maritima) from European coastal regions were evaluated for resistance in controlled environment tests. Quantification of P. betae biomass in seedling roots was achieved using recombinant antibodies raised to a glutathione-s-transferase expressed by the parasite in vivo. Several putative sources of resistance were identified and selected plants from these were hybridized with a male-sterile sugar beet breeding line possessing partial virus resistance (Rz1). Evaluation of F1 hybrid populations identified five in which P. betae resistance had been successfully transferred from accessions originating from Mediterranean, Adriatic and Baltic coasts. A resistant individual from one of these populations was backcrossed to the sugar beet parent to produce a BC1 population segregating for P. betae resistance. This population was also tested for resistance to BNYVV. Amplified fragment length polymorphism and single-nucleotide polymorphism markers were used to map resistance quantitative trait loci (QTL) to linkage groups representing specific chromosomes. QTL for resistance to both P. betae and BNYVV were co-localized on chromosome IV in the BC1 population, indicating resistance to rhizomania conditioned by vector resistance. This resistance QTL (Pb1) was shown in the F1 population to reduce P. betae levels through interaction with a second QTL (Pb2) found on chromosome IX, a relationship confirmed by general linear model analysis. In the BC1 population, vector-derived resistance from wild sea beet combined additively with the Rz1 virus resistance gene from sugar beet to reduce BNYVV levels. With partial virus resistance already deployed in a number of high-yielding sugar beet cultivars, the simple Pb1/Pb2 two-gene system represents a valuable additional target for plant breeders.