Salmonella enterica serovar Napoli (S. Napoli) was first isolated from a human stool in 1945 in Naples (Italy)1. Since the mid-1990s’, the number of human infections caused by the serovar Napoli has progressively increased in Europe, especially in Italy, Switzerland and France2. Unlike all major nontyphoidal Salmonella serovars, serovar Napoli is rarely associated with food-borne outbreaks and is likely an environmental pathogen. Unfortunately, until today and despite several attempts, no study succeeded in identifying the natural source for this serovar, thus preventing public health agencies to propose any prophylactic measures. As a first step towards the understanding of the natural ecology of serovar Napoli, we investigated S. Napoli’s population diversity in its entire distribution area, namely Italy, Switzerland and France. In order to carry out an evolutionary genomics study, we performed whole-genome sequencing (WGS) on 1200 isolates collected between 1945 and 2021 in Italy, Switzerland and France, from human, animal and environmental sources. As in former WGS studies based on local sampling in Italy3,4, we recorded a surprisingly high genetic diversity for S. Napoli. The hierarchical clustering of the core genome multilocus sequence typing (HierCC of cgMLST5) analysis revealed that S. Napoli’s diversity splits into five main HC900 groups, among which one, the group HC900 1543, is the most prevalent in the three countries, and four are mostly restricted to in Italy and Switzerland. Aiming at analysing the evolutionary events in the core genome (i.e. SNPs, InDels) of the most prevalent HC900 group, we generated a genome of reference for the HC1543 group using PacBio sequencing technology. We identified a strong phylogeographical pattern of S. Napoli, both between countries and within France, irrespective of the isolates’ origin (human, animal or environmental). This study is the most comprehensive genomic analysis for the serovar Napoli populations to date. Our results strongly suggests that local environment is a key determinant in the transmission of S. Napoli to humans. Consequently, the evaluation of the epidemical risks associated to the rise of S. Napoli in Europe will require a One-Health approach, especially combining epidemiology, ecology and genomics.