Abstract <p>The <i>Tc1/mariner</i> superfamily of DNA transposons is one of the most widespread among eukaryotes. In this study, the evolutionary dynamics and transcriptional activity of <i>Tc1/mariner</i> elements in different individuals of the Pacific oyster <i>Magallana</i> (<i>Crassostrea</i>) <i>gigas</i> (Thunberg, 1793) were studied. Analysis of transcriptional activity showed that the transposase gene was expressed in more than half of the <i>Tc1/mariner</i> transposons, and in some cases, at a high level. Manifestations of the dependence of the gene activity level on environmental conditions, developmental stages, and tissues were also observed. Data on the evolutionary dynamics showed that despite the presence of potentially functional copies in more than half of the Tc1/mariner transposons, only a few elements exhibited transposition activity in the recent past. The following scenarios are considered: (1) the activity of oyster <i>Tc1/mariner</i> transposons is strictly suppressed by RNA interference and more extreme and/or prolonged exposure to stressors is needed to overcome its pressure; (2)&#xa0;during oyster evolution, <i>Tc1/mariner</i> transposons accumulated mutations that did not alter the protein structure, but weakened or made the DNA-binding and/or catalytic domains non-functional, so the promoters were still active (transcription occurred), but the transposase appeared to be not able to perform transposition. Since individual elements are constantly in a transcriptionally active state, it is quite possible that the combination of favorable factors can lead to transpositions. The study of the evolutionary dynamics of TEs at the intraspecific level contributes to understanding the mechanisms of evolution and the population genetic structure.</p>