The role of exhibition swine in influenza A virus (IAVs) transmission was recently demonstrated by over 300 human infections of H3N2v viruses while attending agricultural fairs. Through active IAV surveillance in US exhibition swine and whole-genome sequencing of 380 isolates, we demonstrate that exhibition swine are actively involved in the evolution of IAVs, including zoonotic strains. First, frequent introduction of IAVs from commercial swine populations provides new genetic diversity in exhibition pigs each year locally. Second, genomic reassortment between viruses co-circulating in exhibition swine increases viral diversity. Third, viral migration between exhibition swine in neighboring states demonstrates that movements of exhibition pigs contributes to the spread of genetic diversity. The unexpected frequency of viral exchange between commercial and exhibition swine raises questions about the understudied interface between these populations. Overall, the complexity of viral evolution in exhibition swine indicates novel viruses are likely to continually re-emerge, presenting threats to humans