Nuclear reactors waters are typically maintained in ultrapure state and are exposed to varying levels of radiation. Despite the extremely challenging conditions, microorganisms have been previously detected in these environments. The aim of this work was to investigate the bacterial communities in different waters of the BR2 nuclear reactor at SCK CEN, with a particular focus on the basin surrounding the reactor vessel. First, we investigated the viable microbial population in various water bodies using a cultivation-based approach. This yielded an extensive strain collection of 33 bacterial species. One of the isolated strains, Sphingomonas melonis, was shown to be somewhat radiation-resistant, as it survived a radiation dose of 2.1 kGy. Next, we characterized the long-term community dynamics in the basin through 16S rRNA amplicon sequencing. This resulted in the characterization of a diverse bacterial population displaying clear shifts in community profiles: cycles of operation were mostly dominated by an unclassified Gammaproteobacterium and Pelomonas, whereas Methylobacterium prevailed during shutdowns. Finally, we studied the functional characteristics of the microbial community in the basin through shotgun metagenomics. Several pathways with a role in cell function recovery after irradiation were more highly represented during shutdowns. Furthermore, two MAGs were almost entirely reconstructed from the metagenome, namely Bradyrhizobium sp. BTAi1 and Methylobacterium sp. UNC378MF. In conclusion, we managed to uncover a large bacterial diversity in various waters of the BR2, which were shown to harbor significant evolutionary adaptations allowing them to survive in these extremely challenging environments.