The WRKY family of transcription factors play conserved roles in regulating plant growth and stress acclimation. In Populus × canescens , however, the functions of these regulators remain largely unexplored. Through a genome-wide approach, we identified 101 WRKY genes in this species, which were phylogenetically grouped into three main clades and further divided into nine subfamilies, with members spanning all 19 chromosomes. Expression profiling analysis revealed that 33 members responded to salinity, among which PcWRKY1 showed strong induction. Functional analysis demonstrated that overexpression of PcWRKY1 significantly improved salt tolerance. This was achieved via a coordinated mechanism that involves enhanced root Na + exclusion to maintain ionic balance, along with the activation of key antioxidant enzymes, including superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), to alleviate oxidative damage, ultimately sustaining root growth under saline conditions. Together, our study expands the genomic understanding of the WRKY family in poplar and positions PcWRKY1 as a candidate gene for improving salt tolerance in woody plants.