Sugarcane root system comprises of superficial sett roots as well as deeply-penetrating shoot borne roots (SBR) with latter being the permanent root system. In sugarcane, the healthy SBR contributes to a better crop yield and it also helps to produce multiple ratoon crops after the harvest. There is a dearth of in-depth knowledge on SBR system architecture and its functional role in modern day commercial hybrids. A comprehensive phenotypic, anatomical and whole transcriptome profiling, conducted between the commercial sugarcane hybrids and a wild germplasm Erianthus, found a developmental delay in both initiation and establishment of the SBR in commercial hybrid compared to Erianthus. The SBR system in Erianthus proved to be an extensive drought-adaptive root system architecture that significantly contributes to drought tolerance. On the other hand, SBRs in the commercial hybrids showed an irreversible collapse and damage of the root cells under drought stress. The outcomes from the comparative analysis of the transcriptome data showed a significant upregulation of the genes that regulate important stress signalling pathways viz., sugar, calcium, hormone signalling and phenylpropanoid biosynthesis in the SBRs of Erianthus. It was found that through these key signalling pathways, Erianthus SBRs triggered the downstream signalling cascade to impart physiological responses like osmoprotection, modification of the cell walls, detoxification of reactive oxygen species, expression of drought responsive transcription factors, maintenance of cell stability and lateral root development. The current study forms a basis for further exploration of the Shoot Borne Root system as a valuable breeding target to develop drought tolerant sugarcane genotypes.