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European red clover (Trifolium pratense) crops are challenged by clover rot, a devastating disease caused by Sclerotinia trifoliorum or, in some cases by S. sclerotiorum. No completely resistant cultivars are available and resistance breeding is hampered by the lack of knowledge on the number of involved resistance genes and the heritability of clover rot resistance. In this study, we estimated the number of major genes contributing to clover rot resistance by analysing 15 F1 progeny populations from pair crosses between ramets of resistant and susceptible genotypes. Parent plants were chosen from diverse, diploid populations, including wild material, landraces and cultivars. Young progeny plants were inoculated with ascospores, evaluated phenotypically and the segregation of disease scores was studied. Our results indicated that clover rot resistance may be conferred by three major effect genes, although segregation patterns suggested that there may be numerous minor effect genes involved as well. No proof was found for a maternal inheritance of clover rot resistance. To get insight in the heritability of clover rot resistance, we applied divergent selection by our high-throughput bio-test on an experimental diploid population: the original population (70.5 %), the first generation after selection for susceptibility (79.2 %) and the first generation after selection for resistance (62.3 %) differed significantly in susceptibility (p < 0.001). The second generation after selection for resistance (60.0 %) was not more resistant than the first generation after selection for resistance. In the first generation of selection the heritability (h2) was on average 0.34. In the second generation of selection h2 was 0.07. These findings have important implications for resistance breeding.