Mangroves, due to their unique habitats, endure dual stressors from land to ocean and ocean to land directions. While extensive research has been conducted on land-ocean stressors, studies on ocean-land stressors like upwelling are considerably scarce. In this study, ecophysiological, transcriptome, and metabolome analyses were conducted to determine the responses of mangrove plant (Bruguiera gymnorhiza, B. gymnorhiza) to upwelling stress. The results suggested that upwelling stress in B. gymnorhiza induces oxidative stress and membrane damage, which is mitigated by the synergistic actions of antioxidant enzymes and osmoprotectants. Transcriptomic and metabolomic analysis revealed that upregulated genes related to oxidation-reduction and carbohydrate metabolism, along with accumulated metabolites such as amino acids, lipids, phenols, and organic acids, contribute to enhancing antioxidant capacity and maintaining osmotic balance. Further analysis identified key KEGG pathways involved in the response to upwelling stress, including amino acid metabolism, carbohydrate and energy metabolism, flavonoid biosynthesis, and plant hormone signal transduction. These findings provide vital information into the multi-level response mechanisms of mangrove plants to upwelling stress.