Root system architecture (RSA), the distribution of roots in soil, plays a major role in plant survival. RSA is shaped by processes largely governed by the phytohormone auxin. However, auxin has a central role in numerous other processes and it is unclear which molecular mechanisms allow for the regulation of RSA independently of the numerous other processes that are impacted by auxin. Taking advantage of the remarkable natural genetic variation of Arabidopsis thaliana, chemical perturbation of the auxin pathway, and genome wide association mapping, we identify a subunit of a highly conserved molecular complex, the EXOCYST, as a modulator of the auxin pathway. Importantly, the auxin modulatory function of this gene is highly specific for root traits and enables specific regulation of RSA without notably affecting above ground plant traits. At the molecular level, it is acting on the protein distribution of a specific auxin efflux carrier. At the organismal level, allelic variation and genetic perturbation of the EXOCYST subunit lead to alteration of the orientation of root growth and root branching, resulting in a switch from a shallow to a deep root system. Finally, the distribution of alleles of this EXOCYST subunit in natural Arabidopsis populations is highly correlated with precipitation seasonality, suggesting an adaptive role in areas with variable rainfall patterns. We corroborate this idea by showing that overexpression and allelic variation of this EXOCYST subunit affect drought resistance in controlled conditions.