Reaumuria trigyna is an endangered recretohalophyte and a small archaic feral shrub that is endemic to arid and semiarid plateau regions of Inner Mongolia, China. Based on transcriptomic data, we isolated a high-affinity potassium transporter gene (RtHKT1) from R. trigyna, which encoded a plasma membrane-localised protein. RtHKT1 was rapidly upregulated by high Na⁺ or low K⁺ and exhibited different tissue-specific expression patterns before and after stress treatment. Transgenic yeast showed tolerance to high Na⁺ or low K⁺, while transgenic Arabidopsis exhibited tolerance to high Na⁺ and sensitivity to high K⁺, or high Na⁺-low K⁺, confirming that Na⁺ tolerance in transgenic Arabidopsis depends on a sufficient external K⁺ concentration. Under external high Na⁺, high K⁺, and low K⁺ conditions, transgenic yeast accumulated more Na⁺-K⁺, Na⁺, and K⁺; while transgenic Arabidopsis accumulated less Na⁺-more K⁺, more Na⁺, and more Na⁺-K⁺, respectively; indicating that the ion transport properties of RtHKT1 depend on the external Na⁺-K⁺ environment. Salt stress induced upregulation of some ion-transporter genes (AtSOS1/AtHAK5/AtKUP5-6), as well as downregulation of some genes (AtNHX1/AtAVP1/AtKUP9-12), revealing that multi-ion-transporter synergism maintains Na⁺/K⁺ homeostasis under salt stress in transgenic Arabidopsis. Overexpression of RtHKT1 enhanced K⁺ accumulation and prevented Na⁺ transport from roots to shoots, improved biomass accumulation and chlorophyll content in salt-stressed transgenic Arabidopsis. The proline content and RWC increased significantly, and some proline biosynthesis genes (AtP5CS1-2) were also upregulated in salt-stressed transgenic plants. These results suggest that RtHKT1 confers salt tolerance on transgenic Arabidopsis by maintenancing Na⁺/K⁺ homeostasis and osmotic homeostasis.