The influenza A H1N1pdm09 virus continues to pose a significant zoonotic threat, with implications for both animal and human health. Italy, which hosts one of the largest swine populations in Europe, is strategically positioned to monitor the evolution of influenza viruses in livestock. This study addresses the genetic diversity and transmission dynamics of H1N1pdm09 in Italian swine, using whole-genome sequencing and dynamic modelling of samples collected from farms across the country. Our findings indicate multiple independent introductions of H1N1pdm09 into Italy. While most were self-limiting, six distinct transmission clusters suggest localized and sustained spread across various regions. Although many introductions were contained, certain lineages demonstrated the ability to circulate within specific areas. Selective pressure analyses showed strong purifying selection across most viral genes in both swine and human hosts, with non-synonymous to synonymous substitution rate (dN/dS) ratios well below 1. The haemagglutinin gene exhibited a higher dN/dS ratio in swine (~0.28) than in humans (~0.22), indicating slightly relaxed selection in swine. Neuraminidase and non-structural proteins were similarly constrained in both hosts. This study underscores the importance of ongoing genomic surveillance to detect viral circulation and mitigate zoonotic risks. Italy´s contribution supports global influenza monitoring and reinforces the need for a One Health approach that integrates human, animal and environmental health. These insights are crucial for informing public health strategies and improving preparedness for future outbreaks.