Phoma betae is an important seedborne pathogen of table beet worldwide that is capable of causing foliar, root, and damping-off diseases. Ten microsatellite and mating type markers were developed to investigate the genetics of P. betae populations in table beet root crops in New York and in table beet seed crops in Washington, from where table beet seed is predominantly sourced. The markers were used to characterize 175 isolates comprising five P. betae populations (two from New York and three from Washington), and they were highly polymorphic with an allelic range of 4 to 33 and an average of 11.7 alleles per locus. All populations had high genotypic diversity (Simpson's complement index = 0.857 to 0.924) and moderate allelic diversity (Nei's unbiased gene diversity = 0.582 to 0.653). Greater differentiation observed between populations from the two states compared with populations within the same state suggested that an external inoculum source, such as windblown ascospores, may be homogenizing the populations. However, most genetic diversity (87%) was among individual isolates within populations (pairwise index of population differentiation = 0.127; P = 0.001), suggesting that local within-field inoculum source(s), such as infested field debris or infected weeds, may also be important in initiating disease outbreaks. Standardized index of association, proportion of compatible pairs of loci, and mating type ratio calculations showed evidence for a mixed reproduction mode in all populations. These findings could be useful in designing more effective management strategies for diseases caused by P. betae in table beet production.