High salinity is one of the major limiting factors that reduces crop productivity and quality. Herein, we report that small SALT TOLERANCE ENHANCER1 (STE1) protein without any known conserved domains is required for tomato salt tolerance. Overexpression (OE) of SlSTE1 enhanced the tolerance to multiple chloride salts (NaCl, KCl and LiCl) and oxidative stress, along with elevated antioxidant enzyme activities, increased ABA and chlorophyll contents, and reduced MDA and ROS accumulations compared to that of WT plants. Moreover, decreased K+ efflux and increased H+ efflux were detected in the OE plants, which induced a higher K+/Na+ ratio. In contrast, SlSTE1-RNAi plants displayed decreased tolerance to salt stress. RNA-seq data revealed 1330 DEGs in the OE vs WT plants under salt stress, and the transcription of numerous and diverse genes encoding TFs, stress-related proteins, secondary metabolisms, kinases and proteins related to hormone synthesis/signalling (notably ABA and ACC), etc. was greatly elevated. Furthermore, SlSTE1-OE plants showed increased sensitivity to ABA, and the results suggest that SlSTE1 promotes ABA-dependent salt stress-responsive pathways by interacting with SlPYLs and SlSnRK2s. Collectively, our findings reveal that the small SlSTE1 protein confers salt tolerance via ABA signalling and ROS scavenging and improves ion homeostasis in tomato.