Salinity stress includes both osmotic and ionic toxicity. Sodium homeostasis is influenced by Na+ uptake and extrusion, vacuolar Na+ compartmentation and root to shoot Na+ translocation via transpiration. The knockout mutant of the Arabidopsis heterotrimeric G‐protein Gβ subunit, agb1, is hypersensitive to salt, exhibiting a leaf bleaching phenotype. We show that AGB1 is mainly involved in the ionic toxicity component of salinity stress and plays roles in multiple processes of Na+ homeostasis. agb1 mutants accumulate more Na+ and less K+ in both shoots and roots of hydroponically grown plants, as measured by inductively coupled plasma atomic emission spectrometry. agb1 plants have higher root to shoot translocation rates of radiolabelled 24Na+ under transpiring conditions, as a result of larger stomatal apertures and increased stomatal conductance. 24Na+ tracer experiments also show that 24Na+ uptake rates by excised roots of agb1 and wild type are initially equal, but that agb1 has higher net Na+ uptake at 90 min, implicating possible involvement of AGB1 in the regulation of Na+ efflux. Calcium alleviates the salt hypersensitivity of agb1 by reducing Na+ accumulation to below the toxicity threshold. Our results provide new insights into the regulatory pathways underlying plant responses to salinity stress, an important agricultural problem.