The halophyte Aster tripolium, unlike well-studied non-halophytic species, partially closes its stomata in response to high Na+ concentrations. Since A. tripolium possesses no specific morphological adaptation to salinity, this stomatal response, preventing excessive accumulation of Na+ within the shoot via control of the transpiration rate, is probably a principal feature of its salt tolerance within the shoot. The ionic basis of the stomatal response to Na+ was studied in guard cell protoplasts from A. tripolium and from a non-halophytic relative, Aster amellus, which exhibits classical stomatal opening on Na+. Patch-clamp studies revealed that plasma membrane K+ channels (inward and outward rectifiers) of the halophytic and the non-halophytic species are highly selective for K+ against Na+, and are very similar with respect to unitary conductance and direct sensitivity to Na+. On the other hand, both species possess a significant permeability to Na+ through non-rectifying cation channels activated by low (physiological) external Ca2+ concentrations. Finally, it appeared that the differential stomatal response between the two species is achieved, at least in part, by a Na+-sensing system in the halophyte which downregulates K+ uptake. Thus, increases in guard cell cytosolic Na+ concentration in A. tripolium but not in A. amellus, lead to a delayed (20–30 min) and dramatic deactivation of the K+ inward rectifier. This deactivation is probably mediated by an increase in cytosolic Ca2+ since buffering it abolishes the response. The possible role of K+ inward rectifiers in the response of A. tripolium’s stomata to Na+, suggested by patch-clamp studies, was confirmed by experiments demonstrating that specific blockade of inward rectifying channels mimics Na+ effects on stomatal aperture, and renders aperture refractory to Na+.