Abstract: This study aimed to screen “Antioxidant+Whitening” dual-function peptides from Morchella esculenta using bioinformatics methods, verify their efficacy, and explore their potential mechanisms of action. Through the integrated application of bioinformatics approaches including virtual enzymatic hydrolysis, activity prediction, physicochemical property and safety assessment, and molecular docking, four peptides from M. esculenta with potential “antioxidant+whitening” effects were were virtually screened as follows: WWVCAK, WWV, RARW, and VMRWKP. In vitro experiments confirmed that the hexapeptide WWVCAK exhibits better antioxidant activity and tyrosinase inhibitory activity. Cell experiments further revealed that WWVCAK can significantly enhance the total antioxidant capacity of B16F10 cells, reduce intracellular reactive oxygen species (ROS), malondialdehyde (MDA), and melanin levels, and effectively inhibit intracellular tyrosinase activity. Network pharmacology research indicated that SRC, HDAC1, ITGB2, ITGB1, PLG, MMP2, MMP9, HDAC2, ITGB3, and ITGAL are key targets of the “antioxidant+whitening” effects of WWVCAK. The peptide exerts its dual activity by participating in various biological processes including proteolysis, organization and disassembly of extracellular matrix, and collagen catabolic process, as well as by regulating multiple signaling pathways such as neuroactive ligand-receptor interaction, neutrophil extracellular trap formation, and leukocyte transendothelial migration. In conclusion, WWVCAK is a bioactive peptide with promising “antioxidant+whitening” properties and thus has potential for further development and application.