Elevated sodium (Na⁺) decreases plant growth and, thereby, agricultural productivity. The ion transporter high-affinity K⁺ transporter (HKT)1 controls Na⁺ import in roots, yet dysfunction or overexpression of HKT1 fails to increase salt tolerance, raising questions as to HKT1's role in regulating Na⁺ homeostasis. Here, we report that tissue-specific regulation of HKT1 by the soil bacterium Bacillus subtilis GB03 confers salt tolerance in Arabidopsis thaliana. Under salt stress (100 mM NaCl), GB03 concurrently down- and upregulates HKT1 expression in roots and shoots, respectively, resulting in lower Na⁺ accumulation throughout the plant compared with controls. Consistent with HKT1 participation in GB03-induced salt tolerance, GB03 fails to rescue salt-stressed athkt1 mutants from stunted foliar growth and elevated total Na⁺ whereas salt-stressed Na⁺ export mutants sos3 show GB03-induced salt tolerance with enhanced shoot and root growth as well as reduced total Na⁺. These results demonstrate that tissue-specific regulation of HKT1 is critical for managing Na⁺ homeostasis in salt-stressed plants, as well as underscore the breadth and sophistication of plant–microbe interactions.