The ERF transcription factor (TF) family performs a central function in plant adaptation to abiotic stress. This study identified 66 ZoERF genes in the ginger (Zingiber officinale Roscoe), phylogenetically classified into six subgroups. Collinearity analysis showed that segmental duplication is the primary driver in ZoERF expansion and demonstrated ginger's closer evolutionary affinity to monocots than dicots. Promoter analysis indicated 43 TF binding sites across the family, highlighting complex transcriptional networks governing stress responses. Under high temperature and high humidity (HTHH) stress, ZoERF60 showed significant tissue-wide upregulation (roots/stems/leaves), corroborated by HTHH-inducible GUS activity. While also responsive to individual high-temperature (HT) or high-humidity (HH) treatments, ZoERF60 expression was highest under combined HTHH stress. Functional characterization demonstrated that ZoERF60 has nuclear localization and transcriptional self-activation capacity. Yeast one-hybrid assays confirmed that ZoERF60 specifically binds to the GCC-box element, implicating it in the regulation of downstream stress-related genes. Heterologous overexpression of ZoERF60 in tobacco significantly enhanced tolerance to both HT and HTHH stresses through reduced reactive oxygen species accumulation, elevated antioxidant enzyme activities, increased proline (Pro) biosynthesis, and decreased malondialdehyde content. Conversely, virus-induced gene silencing (VIGS) of ZoERF60 in ginger compromised reactive oxygen species (ROS) scavenging and amplified oxidative damage. This study elucidates ZoERF60's role as a master regulator of HTHH resilience and provides a genetic resource for climate-resilient crop development.