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Soybean cyst nematode (SCN, Heterodera glycines Ichinohe) is one of the most economically destructive pathogens. The soybean line Zhongpin03-5373 (ZP), which combines resistance genes from several donors, is highly resistant to SCN race 3 (SCN3). In our previous study, two QTL (rhg1 and GmSNAP11) were identified in a population of recombinant inbred lines derived from a cross between ZP and the susceptible parent Zhonghuang 13. The two QTL explained around one-third of the resistance, suggesting the presence of further QTL contributing to SCN resistance. In the present study, we used an improved version of the genetic map comprising the previously applied 1062 molecular markers and 47 newly developed InDel (insertion-deletion) markers. The improved map revealed a novel locus contributing to SCN3 resistance:qSCN3-1, flanked by InDel marker InDel1-7 and SNP marker Map-0047, explained 4.55％of the phenotypic variance for resistance to SCN3 and was not involved in digenic epistatic interaction with rhg1 and GmSNAP11. Haplotypes of Map-0047_CAPS (a CAPS marker developed for Map-0047) and InDel1-7 were significantly associated with SCN3 resistance in a panel of 209 resistant and susceptible accessions. Using further allele-combination analysis for three functional markers representing three cloned resistance genes (rhg1, Rhg4, and GmSNAP11) and two markers flanking qSCN3-1, we found that adding the resistance allele of qSCN3-1 greatly increased soybean resistance to SCN, even in diverse genetic backgrounds. The qSCN3-1 locus will be useful for marker-assisted polygene pyramid breeding and should be targeted for the future identification of candidate genes.