Aerobic rice production (AP) offers high yield in non-flooded environments with occasional mild intermittent water deficits. To enhance adaptation, advantages of genotypes with narrower root cone angle (RCA) and deeper roots, crucial for AP were investigated. Using four bi-parental populations and a set of diverse japonica genotypes, 15 experiments in field and glasshouse conditions with different water availabilities were conducted to identify and validate genomic regions associated with two key traits, narrow RCA and proportion of deep roots below 20 cm (DR20). Linkage and association mapping identified sixteen genomic regions linked to RCA and DR20. Notably, qRCA4 consistently demonstrated favourable performance across diverse genetic backgrounds, while qADR1 and qADR6 exhibited robust effects across experiments with varying water availability. Four candidate genes for qRCA4, including a putative villin protein implicated in actin regulation, were identified through whole genome resequencing and gene ontology analysis. Additionally, seven KASP markers tagging qRCA4 were developed and validated. Preliminary KASP marker development for DR20 showed promising polymorphism between parental lines, with high call rates and clear clustering. Future experiments will focus on validating the DR20 molecular markers and utilise CRISPR gene editing to aid in identifying the causal gene for qRCA4, qADR1, and qADR6. Adopting a systems biology approach, integrating transcriptomics and metabolomics, holds promise in elucidating genes associated with deeper rooting in AP systems. Findings from this study aim to advance development of climate-smart, sustainably produced rice.