Salt stress is a major environmental factor limiting crop production. High-affinity potassium transporters (HAKs) play a crucial role in environmental adaptation, including salt stress. However, the functional characterization of wheat HAKs in response to salt stress has not yet been reported. In this study, wheat HAK member TaHAK1 was investigated to explore its role in salt stress tolerance. Heterologous expression of TaHAK1 in the R5421 yeast strain revealed that yeast growth expressing TaHAK1 was promoted with increasing K⁺ concentrations (0.1–100 mM), while potassium supplementation mitigated growth inhibition under 100–200 mM Na⁺ concentrations. This indicates that TaHAK1 plays a pivotal role in alleviating high Na⁺ stress. Moreover, TaHAK1-overexpressing transgenic lines in rice significantly increased plant biomass, the content of ascorbic acid and glutathione, and activities of antioxidant enzymes, while markedly reduced malondialdehyde levels. And these rice transgenic lines also maintained higher K⁺ and lower Na⁺ contents, suggesting that TaHAK1 could be essential for an optimal Na⁺/K⁺ ratio in salt tolerance. Furthermore, transcriptomic analysis revealed that differentially expressed genes related to signal transduction, ion transport, and oxidative stress responses were significantly induced under salt stress. Among these, many genes were involved in the auxin signaling pathway, suggesting it may be a key regulatory mechanism through which TaHAK1 mediates salt tolerance. In conclusion, TaHAK1 alleviates salt stress by modulating reactive oxygen species, maintaining K⁺/Na⁺ homeostasis, and up-regulating auxin signaling-related genes. Thus, TaHAK1 holds potential for enhancing salt tolerance in crops and could be utilized in future molecular breeding programs targeting salt stress resilience.