Salinity stress limits plant growth and has a major impact on agricultural productivity. Here, we identify NAC transcription factor SlTAF1 as a regulator of salt tolerance in cultivated tomato (Solanum lycopersicum). While overexpressing SlTAF1 improves salinity tolerance compared to wild type, lowering SlTAF1 expression causes stronger salinity-induced damage. Under salt stress, shoots of SlTAF1 knockdown plants accumulate more toxic Na ions, while SlTAF1 overexpressors accumulate less, in accordance with an altered expression of the Na transporter genes SlHKT1;1 and SlHKT1;2. Furthermore, stomatal conductance and pore area are increased in SlTAF1 knockdown plants during salinity stress, but decreased in SlTAF1 overexpressors. We identified stress-related transcription factor, ABA metabolism, and defense-related genes as potential direct targets of SlTAF1, correlating it with reactive oxygen species (ROS) scavenging capacity and changes in hormonal response. Salinity-induced changes in tricarboxylic acid cycle intermediates and amino acids are more pronounced in SlTAF1 knockdown than wild-type plants, but less so in SlTAF1 overexpressors. The osmoprotectant proline accumulates more in SlTAF1 overexpressors than knockdown plants. In summary, SlTAF1 controls tomato's response to salinity stress by combating both, osmotic and ion toxicity, highlighting it as a promising candidate for the future breeding of stress-tolerant crops.