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The Yesso scallop is a large and ancient molluscan group with great economic value; however, it has recently suffered severe cases of Polydora infection. Polydora parasitizes the shells of scallops, badly damaging shell structures and affecting growth and mortality. To investigate the molecular mechanism of Yesso scallops’ response to Polydora infection, proteomic profiling changes in the mantle tissues of Polydora-infected (diseased) and healthy scallops were systematically analysed by tandem mass tags (TMT) labelling technology in this study. A total of 519 differentially expressed proteins (DEPs) were identified. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed most innated immune-related functions and pathways were significantly downregulated in diseased scallops, except the phagocytosis pathway, indicating an important role of phagocytosis in response to Polydora infection. DEPs involved in the phagocytosis pathway were associated with phagocytic receptor recognition, phagosome biogenesis and pathogen degradation, and they were further verified by quantitative real-time PCR. The results elucidate the molecular components of phagocytosis in molluscs for the first time. Polydora can be encapsulated by melanization with an obvious appearance in shells; indeed, melanization-related DEPs were upregulated in diseased scallops. Inhibition of apoptosis and nervous modulation may be also involved in the response mechanism, with some highly associated proteins significantly differentially expressed. Finally, a protein–protein interaction network was constructed to provide a global view of the interaction relationships of the DEPs. The study predicts the molecular response mechanism of Yesso scallops to Polydora infection, and lays a theoretical foundation for Polydora disease control.