As emerging contaminants, galaxolide (HHCB) and polystyrene microplastics (PSMP) are known to persist in the environment at low concentrations, posing significant ecological risks. While extensive research has focused on their ecotoxicological effects, limited attention has been given to plant tolerance mechanisms. This study investigates the tolerance and adaptive mechanisms of the ornamental plant Mirabilis jalapa L. (M. jalapa) to HHCB and PSMP exposure. Results demonstrated that M. jalapa exhibited robust tolerance to both pollutants, maintaining healthy growth in rhizomes and leaves, as evidenced by increased length and biomass. Exposure to PSMP and HHCB induced stomatal opening and enhanced transpiration, potentially mitigating pollutant toxicity. Both contaminants triggered oxidative stress, but M. jalapa activated defense mechanisms, as indicated by reduced malondialdehyde (MDA) levels and increased superoxide dismutase (SOD) activity, effectively regulating reactive oxygen species (ROS) and maintaining cellular homeostasis. Integrated metabolomic and transcriptomic analyses identified six co-annotated KEGG pathways, involving 11 key genes and 6 metabolites, revealing that M. jalapa employs adaptive energy metabolism and pollutant defense strategies to counteract HHCB and PSMP stress. These findings provide a theoretical foundation for utilizing M. jalapa in phytoremediation of HHCB and/or PSMP contamination.