Given their free-ranging habits, feral swine could serve as reservoirs or spatially dynamic "mixing vessels" for influenza A virus (IAV). To better understand virus shedding patterns and antibody response dynamics in the context of IAV surveillance among feral swine, we used feral swine-origin IAV to perform infection experiments. The virus was highly infectious and transmissible in feral swine, and virus shedding patterns and antibody response dynamics were similar to those in domestic swine. In the virus-inoculated and sentinel groups, virus shedding lasted ≤6 days and ≤9 days, respectively. Antibody titers in inoculated swine peaked at 1:840 on post-inoculation day (DPI) 11, remained there until 21 DPI, and dropped to <1:220 at 42 DPI. Genomic sequencing identified changes in wild-type viruses and isolates from sentinel swine, most notably, an amino acid divergence in nucleoprotein position 473. Using data from cell culture as a benchmark, sensitivity and specificity of a matrix gene-based quantitative RT-PCR method using nasal swab samples for detection of IAV in feral swine were 78.9% and 78.1%, respectively. Using data from hemagglutination inhibition assays as a benchmark, sensitivity and specificity of an ELISA for detection of IAV-specific antibody were 95.4% and 95.0%, respectively. Serological surveillance from 2009 to 2014 showed that about 7.58% of feral swine in the United States were positive for IAV. Our findings confirm the susceptibility of IAV infection and the high transmission ability of IAV among feral swine, and also suggest the need for continued surveillance of IAVs in feral swine populations