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Regulatory variants in gene expression serve as bridges linking genetic variation and phenotypic plasticity. Environmental conditions typically influence the effects of regulatory variants on phenotypic plasticity; however, such genotype-by-environment interactions (G × E) are poorly understood. This study aimed to investigate the genetic basis of G × E in estuarine oyster (Crassostrea ariakensis), which is an important model animal for studying environmental adaption owing to its high plasticity and large intraspecific divergence. Genome-wide mapping of expression quantitative trait loci (eQTLs) for 23 environmental adaptive genes was performed for 256 estuarine oysters. We identified 1194 eQTL single nucleotide polymorphisms (eSNPs), including 433 cis -eSNPs in four genes and 722 trans -eSNPs in eight genes. The expression variation explanation of cis -eSNPs (9.95%) was significantly higher than that of trans -eSNPs (9.15%). We specifically showed cis- and trans-eSNPs with high linkage disequilibrium (LD) for Traf7 , Slc6a5 , Ggt , and Dap3. For example, we identified a cis -regulatory LD block containing 68 cis -eSNP and a trans -regulatory LD block, including 20 trans -eSNPs in Traf7. A high proportion (85%) of 40 vital eSNPs exhibited significant G × E effects. We identified crossing and nonparallel interactions of G × E, with the tag cis -eSNPs of Baat and Slc6a5 as representatives. Our results indicated that cis -eQTLs are highly conserved. This study provides insights into the understanding of adaptive evolutionary mechanisms and phenotypic response prediction to variable environments, as well as the genetic improvement for superior adaptive traits for genetic resource conservation and aquaculture. • We identified trans and cis regulatory variants and built potential regulatory networks. • Cis -eSNPs had larger contributions to gene expression plasticity and are conserved in different environments. • Trans -eSNPs are more abundant than cis -eSNPs and usually environment-specific. • A large proportion of eSNPs exhibited significant G × E effects. • Crossing and nonparallel G × E patterns were identified. [ABSTRACT FROM AUTHOR]