Animal origin influenza viruses pose significant pandemic threats, with swine serving as key hosts. Serological surveillance in pigs remains limited in regions with intense human–animal–avian contact. Between March 2020 and July 2022, we collected 4,089 pig serum samples in Cambodia, of which 1,321 (32.5%) were influenza A virus (IAV) seropositive by ELISA. We developed a multiplex microsphere immunoassay comprising a broad panel of hemagglutinin (HA) and neuraminidase (NA) antigens. Seroprevalence was highest for pandemic H1N1/pdm09 (35.3–45.7%) and lower for classical swine H1 (16.4–17.7%) and European avian-like swine H1 (～15%) lineages. Lineage-specific or shared exposures to multiple lineages were observed, indicating complex infection histories. H3 responses varied by clade, while antibodies to avian H5, H7, and H9 were detected in <8% of IAV-positive sera. These findings underscore ongoing zoonotic risk posed by diverse IAVs circulating in pigs and highlights the need for integrated serological and genomic surveillance.