Soil salinity is a major constraint limiting jujube production in China. Wild jujube (Ziziphus jujuba var. spinosa (Bunge) Hu ex H. F. Chow) is widely used as the rootstock of jujube (Z. jujuba) to overcome the saline conditions. To understand the adaptive mechanism in wild jujube under saline conditions, we combined spatiotemporal and physiological assessments with transcriptomic analysis on wild jujube seedlings undergoing various salt treatments. These salt treatments showed dose and duration effects on biomass, photosynthesis, (K+) and (Na+) accumulation. Salt treatments induced higher levels of salicylic acid in roots and leaves, whereas foliar abscisic acid was also elevated after 8 days. The number of differential expression genes increased with higher doses and also longer exposure of NaCl treatments, with concomitant changes in the enriched Gene Ontology terms that were indicative of altered physiological activities. Gene co-expression network analysis identified the core gene sets associated with salt-induced changes in leaves, stems and roots, respectively. The nitrogen transporters, potassium transporters and a few transcription factors belonging to WRKY/MYB/bHLH families were clustered as the hub genes responding to salt treatments, which were related to elevated nitrogen and K+/Na+. Ectopic overexpression of two WRKY transcription factor genes (ZjWRKY6 and ZjWRKY65) conferred stronger salt-tolerance in Arabidopsis thaliana transformants by enhancing the activities of antioxidant enzymes, decreasing malondialdehyde accumulation and maintaining K+/Na+ homeostasis. This study provided evidence about the spatiotemporal, physiological and transcriptomic dynamics of wild jujube during salt stress and identified potential genes for further research to improve salt tolerance in jujube.