Chicken developmental mutants are valuable for discovering sequences and pathways controlling amniote development. Herein we applied the advanced technologies of targeted sequence genomic capture enrichment and next-generation sequencing to discover the causative element for three inherited mutations affecting craniofacial, limb and/or organ development. Since the mutations (coloboma, diplopodia-1 and wingless-2) were bred into a congenic line series and previously mapped to different chromosomes, each targeted mutant causative region could be compared to that of the other two congenic partners, thereby providing internal controls on a single array. Of the ~73 million 50-bp sequence reads, ~76% were specific to the enriched targeted regions with an average target coverage of 132-fold. Analysis of the three targeted regions (2.06 Mb combined) identified line-specific single nucleotide polymorphism (SNPs) and micro (1-3 nt) indels. Sequence content for regions indicated as gaps in the reference genome was generated, thus contributing to its refinement. Additionally, Mauve alignments were constructed and indicated putative chromosomal rearrangements. This is the first report of targeted capture array technology in an avian species, the chicken, an important vertebrate model; the work highlights the utility of employing advanced technologies in an organism with only a "draft stage" reference genome sequence.