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Cadmium is one of the major heavy metal pollutants in the environment. However, the toxicity targets and response mechanisms in photosynthetic organisms to cadmium are lacking. This study explored the physiological response of <i>Synechocystis</i> sp. PCC 6803 to cadmium stress; the toxicity targets and the resistance mechanism were screened. The results showed that cadmium led to an increase in reactive oxygen species content, superoxide dismutase activity, and the lipid peroxidation level, which damaged the cell’s photosynthesis and ultrastructure. The cross-omics analysis found 1073 differentially expressed genes (DEGs), of which only 84 genes had the same expression trend at the mRNA and protein levels. The bioinformatics analysis found that the toxic effects of cadmium were inhibiting the expression of the proteins for the photosynthesis-antenna, photosynthesis, and ribosome pathway. The cell’s response included the upregulation of proteins related to the two-component system, biosynthesis, and ABC transporter pathway. The study confirmed that the target sites of cadmium were chlorophyll <i>a</i> synthesis, photosynthetic electron transport chains, and ribosomes; the response mechanism to cadmium toxicity was the upregulation of the ABC transporter pathway and its protein expression. This study provides evidence to obtain insight into the toxicity targets and molecular response mechanism of <i>Synechocystis</i> sp. PCC 6803 to cadmium stress.