Aphanomyces euteiches is a major soilborne oomycete pathogen that infects various legume species, including pea and alfalfa. The model legume Medicago truncatula has recently emerged as a valuable genetic system for understanding the genetic basis of resistance to A. euteiches in leguminous crops. The objective of this study was to identify genetic determinants of resistance to a broad host-range pea-infecting strain of A. euteiches in M. truncatula. Two M. truncatula segregating populations of 178 F5 recombinant inbred lines and 200 F3 families from the cross F83005.5 (susceptible) × DZA045.5 (resistant) were screened for resistance to A. euteiches. Phenotypic distributions observed suggested a dominant monogenic control of resistance. A major locus associated with resistance to A. euteiches, namely AER1, was mapped by bulk segregant analysis to a terminal end of chromosome 3 in M. truncatula and explained 88% of the phenotypic variation. AER1 was identified in a resistance-gene-rich region, where resistance gene analogs and genes associated with disease resistance phenotypes have been identified. Discovery of AER1 opens up new prospects for improving resistance to A. euteiches in cultivated legumes using a comparative genomics approach.