Tick-borne pathogens are responsible for many vector-borne diseases in Europe, causing important problems for human and animal health. The composition of viral communities in ticks and their interactions with pathogens is little understood, especially in Eastern Europe, an area that represents a major hub for animal-arthropod vectors exchanges. In this study, we used metatranscriptomics to characterize the virome of 2,753 Ixodes ricinus ticks collected from France and Romania, focusing on viruses that could potentially have implications for human or animal health. Among the great viral diversity of viruses identified, we reported a novel strain of Tribec virus, an important human pathogen that was found in Romanian ticks. We detected viruses belonging to the Phenuiviridae and Nairoviridae families close to human and animal pathogens, suggesting that these viruses could constitute novel arboviruses. We used luciferase immunoprecipitation system targeting external viral proteins of viruses identified among the Sedoreoviridae, Phenuiviridae, and Nairoviridae families to screen serum samples from small ruminants’ exposed to tick bites. The results suggest that part (approximately 12%, 95% CI 9.1–16.2) of the small ruminant population from Danube Delta, was exposed to viruses related to bi- or tri-segmented nairoviruses, but cross-reactive viruses could not be confirmed with certainly. The strategy developed in this study serves as a key step in predicting potential new disease outbreaks and can be readily adapted to study other reservoirs, vectors, and interfaces involving susceptible hosts.