Soybean red crown rot (RCR), a soil-borne disease caused by the fungus Calonectria ilicicola, can lead to annual yield losses of up to 30%. This study identified quantitative trait loci (QTLs) associated with RCR resistance in three wild soybean accessions, ‘Gs-7,’ ‘Gs-9,’ and ‘Gs-27.’ QTL analysis was performed using four populations of recombinant inbred lines (RILs) derived from crossing these wild soybean accessions with two susceptible soybean cultivars ‘Enrei’ (populations En7, En9, and En27, respectively) and ‘Williams 82’ (W9). Genetic linkage maps were constructed using 145–256 simple sequence repeat (SSR) markers for each population, and the RILs were evaluated for RCR resistance in a greenhouse. Consequently, eight QTLs were detected across four regions: qRci1 (En9) and qRci1t (W9) on chromosome 8; qRci2 (En9), qRci2t (En7), and qRci2tw (W9) on chromosome 13; qRci3 (W9) on chromosome 18; qRci4 (En7) and qRci4t (En27) on chromosome 3. Further mapping using residual heterozygous lines localized qRci1 to a 2.52 Mb region between BARCSOYSSR_08_0371 and BARCSOYSSR_08_0507, containing 76 candidate genes. Mapping and QTL-seq analysis suggested that qRci2 was in a 0.90 Mb region downstream of BARCSOYSSR_13_1504, containing 33 candidate genes. Four QTLs—qRci1, qRci2, qRci2t, and qRci4—were backcrossed into ‘Enrei,’ an elite Japanese cultivar, reducing disease severity in both greenhouse and field trials. No epistatic interactions were observed, and two QTLs, qRci2t and qRci4, conferred greater resistance than a single QTL in BC1F4 lines. Thus, pyramiding these QTLs is recommended to confer RCR resistance in commercial soybean cultivars.