Several lineages of influenza A viruses (IAV) currently circulate in North American pigs. Genetic diversity is further increased by transmission of IAV between swine and humans and subsequent evolution. Here, we characterized the genetic and antigenic evolution of contemporary swine H1N1 and H1N2 viruses representing clusters H1-α (1A.1), H1-β (1A.2), H1pdm (1A.3.3.2), H1-γ (1A.3.3.3), H1-δ1 (1B.2.2), and H1-δ2 (1B.2.1) currently circulating in pigs in the United States. The δ1-viruses diversified into two new genetic clades, H1-δ1a (1B.2.2.1) and H1-δ1b (1B.2.2.2), which were also antigenically distinct from the earlier H1-δ1-viruses. Further characterization revealed that a few key amino acid changes were associated with antigenic divergence in these groups. The continued genetic and antigenic evolution of contemporary H1 viruses might lead to loss of vaccine cross-protection that could lead to significant economic impact to the swine industry, and represents a challenge to public health initiatives that attempt to minimize swine-to-human IAV transmission. •Genetic evolution of H1 IAV in the U.S. pig population resulted in seven distinct antigenic clusters.•The H1-δ1 split into 2 new genetic clades, H1-δ1a (1B.2.2.1) and H1-δ1b (1B.2.2.2).•H1-δ1a (1B.2.2.1) and H1-δ1b (1B.2.2.2) were antigenically distinct from prior H1-δ1.•few key amino acid changes were associated with antigenic divergence in H1-δ>1.