Our understanding of the long-term consequences of chronic ionising radiation for living organisms remains scarce. Modern molecular biology techniques are helpful tools for researching pollutant effects on biota. To reveal the molecular phenotype of plants growing under chronic radiation exposure, we sampled Vicia cracca L. plants in the Chernobyl Exclusion Zone and in areas with normal radiation backgrounds. We performed a detailed analysis of soil and gene expression patterns, and made coordinated multi-omics analyses of plant samples, including transcriptomics, proteomics, and metabolomics. Chronic exposure to ionising radiation induced complex and multidirectional changes, including significant alterations in the metabolism and gene expression patterns of irradiated plants. We revealed profound changes in carbon metabolism, nitrogen reallocation, and photosynthesis. These plants were characterised by increased DNA damage, redox imbalance, and stress response reactions. The upregulation of histones, chaperones, peroxidases, and secondary metabolism were noted.