Under saline conditions, plants consistently maintain cytosolic Na+ concentrations between 10 and 30 mM, sequestering excess Na+ to the vacuole. We demonstrate that this cytosolic Na+ homeostasis is regulated by inward Na+-permeable channels and outward Na+:H+ antiporters at both the plasma membrane and tonoplast. Sodium’s interplay with K+ transport adds complexity and selective transport is crucial to avoid conflicting ion fluxes. Our models predict that Na+:H+ antiport regulation at the plasma membrane significantly impacts cytosolic Na+ levels, while channel and antiport regulation are equally important at the tonoplast. The energetic implications of these transport mechanisms are discussed. In contrast to the cytosol, chloroplast Na+ concentrations vary significantly between species and increase with soil salinity, raising questions as to how C4 and CAM plants acquire pyruvate under saline conditions. However, modelling transport activity at the chloroplast membrane requires far more knowledge of the associated transport systems and the chloroplastic Na+ content.