Recent advances in high throughput sequencing (HTS) approaches allowed a broad exploration of viromes from different fungal hosts, unveiling a great diversity of mycoviruses with interesting evolutionary features. The word mycovirus historically applies also to viruses infecting oomycetes but most studies are on viruses infecting fungi, with less mycoviruses found and characterized in oomycetes, particularly in the obligatory biotrophs. We, here, describe the first virome associated to , the causal agent of lettuce downy mildew, which is an important biotrophic pathogen for lettuce production and a model system for the molecular aspects of the plant-oomycetes interactions. Among the identified viruses, we could detect (1) two new negative sense ssRNA viruses related to the yueviruses, (2) the first example of permuted RdRp in a virus infecting fungi/oomycetes, (3) a new group of bipartite dsRNA viruses showing evidence of recent bi-segmentation and concomitantly, a possible duplication event bringing a bipartite genome to tripartite, (4) a first representative of a clade of viruses with evidence of recombination between distantly related viruses, (5) a new open reading frame (ORF)an virus encoding for an RdRp with low homology to known RNA viruses, and (6) a new virus, belonging to riboviria but not conserved enough to provide a conclusive phylogenetic placement that shows evidence of a recombination event between a kitrinoviricota-like and a pisuviricota-like sequence. The results obtained show a great diversity of viruses and evolutionary mechanisms previously unreported for oomycetes-infecting viruses, supporting the existence of a large diversity of oomycetes-specific viral clades ancestral of many fungal and insect virus clades.