Radioactive contamination of the natural areas is one of the most long-lasting anthropogenic impacts on the environment. Scots pine (Pinus sylvestris L.) is a promising organism for radiation-related research because of its high radiosensitivity, but the genome size of Pinacea species has imposed obstacles for high-throughput studies so far. In this work, we conducted the analysis of the de novo assembled transcriptome of Scots pine populations growing in the Chernobyl-affected zone, which is still today contaminated with radionuclides because of the accident at the nuclear power plant in 1986. The transcriptome profiles indicate a clear pattern of adaptive stress response, which seems to be dose-dependent. The transcriptional response indicates a continuous modulation of the cellular redox system, enhanced expression of chaperones and histones, along with the control of ions balance. Interestingly, the activity of transposable element families is inversely correlated to the exposure levels to radiation. These adaptive responses, which are triggered by radiation doses 30 times lower than the one accepted as a safe for biota species by international regulations, suggest that the environmental management in radiation protection should be reviewed.