Determining the genomic organization of the Ovis aries (Ovar) major histocompatibility complex class IIa region is essential for future functional studies related to antigen presentation. In this study, a bacterial artificial chromosome (BAC) library of genomic DNA from peripheral blood leukocytes (PBL) of a Rambouillet ram was constructed, and BAC clone consisting of the major histocompatibility complex (MHC) class II DQB2, DQA2, DQB1, DQA1, and DRB1 loci was identified and completely sequenced. The BAC clone consists of 160,889 bp of finished sequence with the loci arranged in the following order: DQB2, DQA2, DQB1, DQA1, and DRB1 with 14.3, 25, 6.6, and 40.9 Kb spanning between the loci, respectively. All five of these loci were transcribed in the animal used to generate the MHC class II BAC clone. Repeat or retrotransposable elements along with MHC class II cis promoter elements consisting of S, X, and Y boxes were identified in the sequence. In addition, 16 non-coding conserved sequences amongst primates, carnivores, and ruminants were identified (p < 0.001). These conserved sequences include binding sites for transcription factors with known roles in immune cells, and they provide a basis for further functional investigation of the genes in this region. This is the first ruminant finished sequence of the DQB2-DRB1 region, and this sequence information will aid in whole genome and transcriptome analyses of MHC class II.