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Oysters are a keystone species in estuaries and intertidal zones and have important economic and ecological significance; however, worldwide, the dominant aquaculture oyster species suffers from mass mortality owing to anthropogenic impacts and rapid climate change. As a possible solution, inter/intraspecies hybridization is a feasible way to breed new germplasms with genetic improvement and high environmental adaptability. Suminoe oysters (Crassostrea ariakensis) are broadly distributed in the estuaries of China and have evolved strong genetic divergence between the northern and southern populations; therefore, they are ideal candidates to explore intraspecies heterosis and the associated molecular mechanisms. In this study, we performed reciprocal hybridization and examined fitness traits in oysters cultured in both northern and southern habitats. Reciprocal hybrids performed better than inbred populations in both environments, indicating heterosis in Suminoe oysters. Hybrids reared in maternal habitats showed faster growth, higher field survival, and greater aerobic metabolism than alternative hybrid oysters under the same conditions. The transcriptional analysis identified modules related to heterosis and maternal effect, while genes responsible for galactose metabolism, glycolysis/gluconeogenesis, and the tricarboxylic acid cycle were enriched and upregulated in hybrids, especially those in maternal environments. Our findings reveal that accelerated aerobic energy metabolism, which may result from mitonuclear coadaptation, underlies the molecular basis of heterosis and maternal effect in the hybridization of Suminoe oysters. Thus, we provide important insights for the aquaculture management of marine species, revealing that selecting appropriate environments (maternal habitats) is critical for heterosis in cross-breeding. • Hybrids from divergent oyster populations showed heterosis in growth and survival. • Hybrids in maternal habitat exhibited better performance indicating maternal effect. • Accelerated aerobic metabolism underlies heterosis and maternal effect in oyster. • Our findings propose better hybridization breeding of hybrids in maternal habitat. [ABSTRACT FROM AUTHOR]