Human-like swine H3 influenza A viruses (IAV) were detected by the USDA surveillance system. We characterized two novel swine human-like H3N2 and H3N1 viruses with HA genes similar to human seasonal H3 strains and the internal genes closely related to 2009 H1N1 pandemic viruses. The H3N2 NA was of the contemporary human N2 lineage, while the H3N1 NA was of the classical swine N1 lineage. Both viruses were antigenically distant from swine H3 viruses that circulate in the U.S. and from swine vaccine strains, and also showed antigenic drift from human seasonal H3N2. Their pathogenicity and transmission in pigs were compared to a human H3N2 with common HA ancestry. Both swine human-like H3 viruses efficiently infected pigs and transmitted to indirect contacts, whereas the human H3N2 was much less efficient. To evaluate the role of genes from the swine isolates on their pathogenesis, reverse genetics-generated reassortants between the swine human-like H3N1 and the seasonal human H3N2 were tested in pigs. Gene segment contribution to virulence was complex with the swine HA and internal genes showing effect in vivo. The experimental infections indicate that these novel H3 viruses are virulent and can sustain onward transmission in pigs, and the naturally occurring mutations in the HA were associated with antigenic divergence from H3 IAV from human and swine. Consequently, these viruses could have a significant impact on the swine industry if they cause more widespread outbreaks, and the potential risk of these emerging swine IAV to humans should be considered.