The Major Histocompatibility Complex (MHC) is an important component of developing and regulating host immune response. It is a key genomic model region for understanding the evolution of gene families and co-evolution between host and pathogen. However, from Suidae (pigs) and its’ closest living taxa, Tayassuidae(peccaries), which comprise ~30 extant species (mostly wild), only the genome of the domestic pig (Sus scrofa) has been extensively sequenced and annotated. Based on the S. scrofa MHC, it has been suggested that the non-classical class I gene series (MHC Ib) emerged after Suidae diverged from the rest of the artiodactyls. To test this hypothesis, we used DNA sequence capture to generate MHC resources from 12 wild species of Suidae and Tayassuidae. This was done using the S. scrofa MHC as a reference sequence for the design of the capture array and next-generation sequencing. Our results show that: i) the repertoire of MHC non-classical genes MHCIb (and classical MHC Ia) is present in both Suidae and Tayassuidae in contrast with the previous hypothesis; ii) these genes underwent a series of duplications and differentiation before these taxa diverged from the common ancestor more than 35 million years ago; iii) all genes have evolved independently from each other after speciation; and iv), there are genetic patterns of differentiation for most of the MHC Ia and Ib genes between Eurasian and sub-Saharan wild Suidae. These findings improve our understanding of the evolutionary history of these adaptive immune genes and provide genetic resources to investigate the immune response of wild populations to diseases including local adaptation of some taxa to emerging diseases.