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Ubiquitin‐conjugating enzyme (UBC) is a crucial component of the ubiquitin‐proteasome system, which contributes to plant growth and development. While some UBCs have been identified as potential regulators of abiotic stress responses, the underlying mechanisms of this regulation remain poorly understood. Here, we report a cotton (Gossypium hirsutum) UBC gene, GhUBC10‐2, which negatively regulates the salt stress response. We found that the gain of function of GhUBC10‐2 in both Arabidopsis (Arabidopsis thaliana) and cotton leads to reduced salinity tolerance. Additionally, GhUBC10‐2 interacts with glutathione S‐transferase (GST) U17 (GhGSTU17), forming a heterodimeric complex that promotes GhGSTU17 degradation. Intriguingly, GhUBC10‐2 can be self‐polyubiquitinated, suggesting that it possesses E3‐independent activity. Our findings provide new insights into the PTM of plant GST‐mediated salt response pathways. Furthermore, we found that the WRKY transcription factor GhWRKY13 binds to the GhUBC10‐2 promoter and suppresses its expression under salt conditions. Collectively, our study unveils a regulatory module encompassing GhWRKY13–GhUBC10‐2–GhGSTU17, which orchestrates the modulation of reactive oxygen species homeostasis to enhance salt tolerance. Summary statement: GhUBC10‐2 negatively regulates salt tolerance by targeting glutathione S‐transferase U17 (GhGSTU17) for its degradation. GhWRKY13 binds the W‐box of the GhUBC10‐2 promoter to repress GhUBC10‐2 transcription. The GhWRKY13–GhUBC10‐2–GhGSTU17 module offers a guidance for cotton breeding. [ABSTRACT FROM AUTHOR]