Vine growth habit (VGH) is a beneficial phenotype in many wild plants, and is considered an important domesticated-related trait in soybean. However, its genetic basis remains largely unclear. Hence, in the present study we used an integrated strategy combining linkage mapping and population genome diversity analyses to reveal the genetics of VGH in soybean. In this regard, two recombinant inbred line (RIL) populations derived by crossing a common wild soybean genotype (PI342618B) with two cultivated lines viz., NN 86-4 and NN 493-1 were used to map quantitative trait loci (QTL) for VGH. Here, we identified seven and five QTLs at flowering stage (R1) and maturity stage (R8), respectively, and among them qVGH-18-1, qVGH-18-2, qVGH-19-3, qVGH-19-4 were identified as major loci (R2 > 10% and detection time ≥2). However, qVGH-18-2 was considered as a main QTL for VGH being consistently identified in both RIL populations as well as all growth stages and cropping years. Out of all the annotated genes within qVGH-18-2, Glyma18g06870 was identified as the candidate gene and named as VGH1, which was a gibberellin oxidase (GAox) belongs to 2-oxoglutarate-dependent dioxygenase (2- ODD). Interestingly, there was one member of 2-ODD/GAox in qVGH-18-1 and qVGH-19-4 named as VGH2 and VGH3, respectively. Moreover, from sequencing data analysis VGH1 and three other GAox genes were found significantly divergent between vine and erect soybean with FST value larger than 0.25. Hence, GAox was assumed to play a major role in governing inheritance of VGH in soybean. Therefore, elucidating the genetic mechanism of GAox is very useful for exploring VGH and other stem traits, as well as genetic improvement of plant type in soybean.