Swine influenza A viruses (IAV-S) caused the 2009 H1N1 pandemic and pose a future zoonotic and pandemic threat. Vietnam represents a critical hotspot for IAV-S emergence within East and Southeast Asia, with dense swine and human populations and intensive livestock trade. We conducted genomic surveillance of IAV-S in Vietnam during 2020–2024, extending previous surveillance from 2013–2019. We identified multiple co-circulating H1 and H3 clades, including pandemic H1N1, Eurasian avian-like, and European lineages, by conducting phylogenetic analysis of 56 IAV-S isolates (21 H1N1, 31 H1N2, and 4 H3N2). Three H1 clades persisted exclusively in Vietnam, circulating up to 12 years. Phylogeographic analysis revealed multiple independent introduction events from North America, Europe, China, Thailand, and Cambodia. We detected extensive reassortment that frequently involved pandemic H1N1 virus internal genes. We identified several lineage-specific mutations associated with mammalian adaptation. Our findings underscore the ongoing IAV-S evolution and need for sustained surveillance in Vietnam.