Soybean crops face drought as one of their major yield barriers. Dissecting the complete genetic architecture of drought tolerance (DT) is an ongoing challenge for soybean breeders. A half-sib population with 404 lines consisting of two recombinant inbred line (RIL) populations with M8206 as the joint parent (M8206 × TongShan and ZhengYang × M8206) was established and tested for their DT under sand culture. The population was sequenced using RAD-seq (restriction-site-associated DNA sequencing) filtered with minor allele frequency (MAF) ≥ 0.01, and 55 936 single nucleotide polymorphisms (SNPs) were obtained and organized into 6137 SNPLDBs (SNP linkage disequilibrium blocks). The innovative RTM-GWAS (restricted two stage multi-locus genome-wide association study) identified 46 novel QTLs with 107 alleles on an average of 38.67% of the phenotypic variance (PV) collectively for relative plant length (RPL) and relative plant dry weight (RPDW). The identified quantitative trait loci (QTLs) with their corresponding alleles for RPL and RPDW were structured into QTL-allele matrices, showing the DT genetic architecture of the three parents and half-sib population. From the matrices, the possible best genotype was predicted to have their weighted average value (WAV) over two indicators 1.663, while the top 10 optimal crosses among RILs with 95^th percentile WAV was 0.872–0.960, transgressive over the parents (0.469–0.675) but much less than 1.663, depicting further pyramiding potential. From the detected QTL-allele system, 63 potential candidate genes collectively for both RPL and RPDW indicators explaining on average of 26.94% PV were annotated and χ²-tested as a DT potential candidate gene system involving nine biological processes, endorsing the genetic complexity of DT.