The chicken has been widely used in experimental research given its importance to agriculture and its utility as a model for vertebrate biology and biomedical pursuits for over 100 years. Herein we used advanced technologies to investigate the genomic characteristics of specialized chicken congenic genetic resources developed on a highly inbred background. An Illumina 3K chicken single nucleotide polymorphism (SNP) array was utilized to study variation within and among major histocompatibility complex (MHC)-congenic lines as well as investigate line-specific genomic diversity, inbreeding coefficients, and MHC B haplotype-specific GGA 16 SNP profiles. We also investigated developmental mutant-congenic lines to map a number of single-gene mutations using both the Illumina 3K array and a recently developed Illumina 60K chicken SNP array. In addition to identifying the chromosomes and specific subregions, the mapping results affirmed prior analyses indicating recessive or dominant and autosomal or sex chromosome modes of inheritance. Priority candidate genes are described for each mutation based on association with similar phenotypes in other vertebrates. These single-gene mutations provide a means of studying amniote development and in particular serve as invaluable biomedical models for similar malformations found in human.