The pogo superfamily is one of the most common groups of DNA transposons. Ten pogo transposons are known to occur in the genome of the Pacific oyster Crassostrea (Magallana) gigas (Thunberg, 1793). The oyster pogo elements were shown to belong predominantly to three families: pogoR, Passer, and Fot. A genome analysis in five oysters detected nine pogo elements in each oyster, while one element (Mariner-38_CGi) was found in only two genome assemblies. The genome assemblies differed in the copy number and lengths of the pogo transposons and the presence and lengths of inverted repeats. Data on the evolutionary dynamics of the pogo transposons and their low copy number in individual genomes suggested their low activity throughout the life cycle. A transcriptional activity analysis showed that the Mariner-30_CGi and Mariner-34_CGi elements were expressed permanently or in a condition-dependent manner in more than half of the cases. Transcriptional activities of five elements were found to depend on the developmental stage. It was assumed that the elements could have been domesticated by the oyster genome. The study expands the understanding of evolution of the pogo transposons and their role in animal genome diversification.