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Caspases are cysteinyl aspartate-specific proteinases, playing critical roles in apoptotic pathway to induce apoptosis and inflammatory response. In this study, the expanded repertoire of Caspases was revealed in the Pacific oyster Crassostrea gigas , and a total of 30 Caspases were identified from the genomic and stress-induced transcriptomic databases of the Pacific oyster. They were clustered into Cg Caspase-2/9, Cg Caspase-8/10, Cg Caspase-3/6/7, Cg Caspase-Cg, and Cg Caspase-L. Cg Caspase-Cg subgroup was found to be specifically expanded after a positive selection in oyster with average Ka/Ks of 0.50. The mRNA expression of CgCaspase-Cg-5 was found to be obviously induced against various bacterial and viral stimulations or environmental stresses. The relative expression level of CgCaspase-Cg-5 in haemocytes increased and reached the peak at 6 h after Vibrio splendidus stimulation, which was 5.57-fold of that in the control group (p < 0.01). In the oysters whose CgCaspase-Cg-5 expression was knocked down, the mRNA expression of apoptosis-related genes including CgBcl2 , CgBax , CgCaspase3 and CgCaspase9 changed significantly at 12 h after V. splendidus stimulation. The expression of CgBax , CgCaspase3 and CgCaspase9 decreased, which was 0.64-fold (p < 0.05), 0.53-fold (p < 0.05) and 0.62-fold (p < 0.01), while the expression of CgBcl2 increased, which was 2.81-fold (p < 0.01) of that in the EGFP-dsRNA group, respectively. Meanwhile, the apoptotic rate of haemocytes (1.90 ± 0.71%) significantly decreased compared to that in the EGFP-dsRNA group (5.40 ± 0.72%) (p < 0.05), and the histological damages of widened cell spacing, gill filament swelling and loose cytoplasm were observed in the Cg Caspase-Cg-5-knockdown oysters after V. splendidus stimulation. Collectively, Cg Caspase-Cg subgroup was specifically expanded in oyster and some bivalve species, and species-specific Cg Caspase-Cg-5 regulated the mRNA expression of the apoptosis-related genes to induce haemocyte apoptosis in the early stage of immune response. This provided insight into the evolutionary and functional characteristics of Caspase repertoire in the Pacific oyster and highlighted the important role of Cg Caspase-Cg-5 in the response to pathogen infection and environmental stresses. • Five subgroups of Caspases were identified in the Pacific oyster. • Cg Caspase-Cgs were found to expand in the Pacific oyster after a positive selection. • Cg Caspase-Cg-5 was induced against various biotic and abiotic stresses. • The apoptosis-related genes expressed differently in Cg Caspase-Cg-5-RNAi oysters. • Apoptotic rate of haemocytes decreased significantly in Cg Caspase-Cg-5-RNAi oysters. [ABSTRACT FROM AUTHOR]