West Nile virus (WNV), a mosquito-borne orthoflavivirus, represents an increasing public health threat in Europe. In 2025, the virus was detected in four distinct regions of metropolitan France including in the Paris area. Using virus genomic data collected from the human, animal and entomological compartments we characterize the spatial and temporal dynamics of WNV circulation in France from 2022 to 2025 and determine the origin of the virus lineages responsible for the 2025 emergence in Paris. Based on 52 sequences from WNV-positive samples (6 human, 21 veterinary, and 25 entomological samples), we find that WNV-L2 was the only lineage detected in France between 2022 and 2025. In particular, we identify the emergence of WNV-L2 in the Occitanie region —a large area in the south of France bordering Spain and the Mediterranean sea. By applying phylodynamics to WNV L2 sequences from France and Europe, we date the emergence of WNV in Occitanie and link it to recent virus sublineages from Nouvelle-Aquitaine, a region along the Atlantic coast. Further, we show that WNV L2 strains identified in the Provence-Alpes-Côte d’Azur region —situated only 100 km east of Occitanie— represent a distinct sublineage, likely recently introduced from a neighboring region of Italy. Finally, we find that the virus strains from the Paris area all grouped together and also originated from the WNV-L2 clade from the Nouvelle-Aquitaine region. These findings mark a turning point in the epidemiology of West Nile virus in Europe, highlighting the urgent need to reinforce integrated surveillance systems across all regions —not only where the virus has historically circulated or recently emerged, but more broadly to anticipate and respond to future spread.