The 2009 swine-origin H1N1 influenza A (S-OIV) epidemic emerged in Mexico and the United States in March and early April 2009, spreading to 30 countries within weeks. The World Health Organization raised its pandemic alert to level 5. This study uses evolutionary analysis to trace the origins and early development of the S-OIV epidemic. The virus was derived from several circulating swine viruses, with initial human transmission occurring months before the outbreak was recognized. Phylogenetic analysis suggests a long period of unsampled ancestry, indicating that reassortment of swine lineages may have occurred years before human infection. The multiple genetic ancestry of S-OIV does not indicate an artificial origin. The study highlights the need for systematic surveillance of influenza in swine and provides evidence that the mixing of new genetic elements in swine can lead to pandemic emergence in humans. The S-OIV outbreak's genetic characterization suggested swine as its probable source, with classical swine H1N1 viruses circulating for at least 80 years. The study's phylogenetic analyses show that each segment of the S-OIV genome nested within a well-established swine influenza lineage, suggesting that the epidemic originated in pigs. The long, unsampled history of the epidemic means that the nature and location of the genetically closest swine viruses provide little about the immediate origin of the outbreak. The study also found no evidence of virulence-associated variation or adaptations to human hosts, consistent with the outbreak being of swine origin and causing relatively mild symptoms. The high non-synonymous to synonymous substitution rate ratio in the outbreak clade may be due to increased detection of mildly deleterious mutations or adaptive evolution. The movement of live pigs between Eurasia and North America facilitated the mixing of diverse swine influenza viruses, leading to the multiple reassortment events associated with the genesis of the S-OIV strain.The 2009 swine-origin H1N1 influenza A (S-OIV) epidemic emerged in Mexico and the United States in March and early April 2009, spreading to 30 countries within weeks. The World Health Organization raised its pandemic alert to level 5. This study uses evolutionary analysis to trace the origins and early development of the S-OIV epidemic. The virus was derived from several circulating swine viruses, with initial human transmission occurring months before the outbreak was recognized. Phylogenetic analysis suggests a long period of unsampled ancestry, indicating that reassortment of swine lineages may have occurred years before human infection. The multiple genetic ancestry of S-OIV does not indicate an artificial origin. The study highlights the need for systematic surveillance of influenza in swine and provides evidence that the mixing of new genetic elements in swine can lead to pandemic emergence in humans. The S-OIV outbreak's genetic characterization suggested swine as its probable source, with classical swine H1N1 viruses circulating for at least 80 years. The study's phylogenetic analyses show that each segment of the S-OIV genome nested within a well-established swine influenza lineage, suggesting that the epidemic originated in pigs. The long, unsampled history of the epidemic means that the nature and location of the genetically closest swine viruses provide little about the immediate origin of the outbreak. The study also found no evidence of virulence-associated variation or adaptations to human hosts, consistent with the outbreak being of swine origin and causing relatively mild symptoms. The high non-synonymous to synonymous substitution rate ratio in the outbreak clade may be due to increased detection of mildly deleterious mutations or adaptive evolution. The movement of live pigs between Eurasia and North America facilitated the mixing of diverse swine influenza viruses, leading to the multiple reassortment events associated with the genesis of the S-OIV strain.