Abstract Giant viruses are abundant in aquatic environments and ecologically important through the metabolic reprogramming of their hosts. Less is known about giant viruses from soil even though two of them, belonging to two different viral families, were reactivated from 30,000-y-old permafrost samples. This suggests an untapped diversity of Nucleocytoviricota in this environment. Through permafrost metagenomics we reveal a unique diversity pattern and a high heterogeneity in the abundance of giant viruses, representing up to 12% of the sum of sequence coverage in one sample. Pithoviridae and Orpheoviridae -like viruses were the most important contributors. A complete 1.6 Mb Pithoviridae -like circular genome was also assembled from a 42,000-y-old sample. The annotation of the permafrost viral sequences revealed a patchwork of predicted functions amidst a larger reservoir of genes of unknown functions. Finally, the phylogenetic reconstructions not only revealed gene transfers between cells and viruses, but also between viruses from different families.