Salinity is a devastating abiotic stress accounting for major crop losses yearly. Plant roots can strikingly grow away from high-salt patches. This response is termed halotropism and occurs through auxin redistribution in roots in response to a salt gradient. Here, a natural variation screen for the early and NaCl-specific halotropic response of 333 Arabidopsis accessions revealed quantitative differences in the first 24 h. These data were successfully used to identify genetic components associated with the response through Genome-Wide Association Study (GWAS). Follow-up characterization of knockout mutants in Col-0 background confirmed the role of transcription factor WRKY25, cation-proton exchanger CHX13, and a gene of unknown function DOB1 (Double Bending 1) in halotropism. In chx13 and dob1 mutants, ion accumulation and shoot biomass under salt stress were also affected. Thus, our GWAS has identified genetic components contributing to main root halotropism that provide insight into the genetic architecture underlying plant salt responses.