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Heavy metal copper (Cu) will inevitably impact the marine macroalgae <i>Gracilariopsis lemaneiformis</i> (<i>G. lemaneiformis</i>), which is a culture of economic importance along China’s coastline. In this study, the detoxification mechanism of Cu stress on <i>G. lemaneiformis</i> was revealed by assessing physiological indicators in conjunction with transcriptome and metabolome analyses at 1 d after Cu stress. Our findings revealed that 25 μM Cu stimulated ROS synthesis and led to the enzymatic oxidation of arachidonic acid residues. This process subsequently impeded <i>G. lemaneiformis</i> growth by suppressing photosynthesis, nitrogen metabolism, protein synthesis, etc. The entry of Cu ions into the algae was facilitated by ZIPs and IRT transporters, presenting as Cu²⁺. Furthermore, there was an up-regulation of Cu efflux transporters HMA5 and ABC family transporters to achieve compartmentation to mitigate the toxicity. The results revealed that <i>G. lemaneiformis</i> elevated the antioxidant enzyme superoxide dismutase and ascorbate-glutathione cycle to maintain ROS homeostasis. Additionally, metabolites such as flavonoids, 3-O-methylgallic acid, 3-hydroxy-4-keto-gama-carotene, and eicosapentaenoic acid were up-regulated compared with the control, indicating that they might play roles in response to Cu stress. In summary, this study offers a comprehensive insight into the detoxification mechanisms driving the responses of <i>G. lemaneiformis</i> to Cu exposure.