Cold stress restricts plant development seriously, resulting in heavy agricultural losses. We found a critical transcription factor network in Medicago ruthenica is involved in plant adaptation to low temperature. APETALA2/ETHYLENE RESPONSIVE FACTOR (AP2/ERF) transcription factor MrERF039 was transcriptionally induced by cold stresses in M. ruthenica. We established an agrobacterium-mediated transient expression system and found that MrERF039 plays an active role in the cold response of M. ruthenica. Overexpression of MrERF039 significantly increased the soluble sugar content, which was eventually expressed as the accumulation of glucose and maltose. Electrophoretic mobility shift assays (EMSA) and yeast monohybrid crosses showed that MrERF039 could bind to the DRE cis-acting element on the MrCAS15A promoter. Additionally, the methyl group of the 14th amino acid in the MrERF039 protein was required for the binding. Transcriptome results analysis showed that the MrERF039 gene acted as a sugar molecular switch, regulating many sugar transporters and sugar metabolism related genes. In addition, we found that MrERF039 can directly regulate the expression of β-amylase gene, UDP glycosyltransferase gene and C2H2 zinc finger protein gene. And the significant increase in glucose and maltose content may be caused by the breakdown of starch degraded by β-amylase. In conclusion, these findings suggest that high expression of the MrERF039 gene can significantly improve the cold tolerance of M. ruthenica root tissues during cold acclimation. These provides a new theoretical basis and candidate genes for breeding new legume forage varieties with high resistance, high yield and high protein.