Most recent initiatives to sequence and assemble new species’ genomes de-novo fail to achieve the ultimate endpoint to produce a series of contigs, each representing one whole chromosome. Even the best-assembled genomes (using contemporary technologies) consist of sub-chromosomal sized scaffolds. To circumvent this problem, we developed a novel approach that combines computational algorithms to merge scaffolds into chromosomal fragments, scaffold verification by PCR and physical mapping to chromosomes. Multi genome-alignment-guided probe selection led to the development of a set of universal avian BAC clones that permit rapid anchoring of multiple scaffold loci to chromosomes on all avian genomes. As proof of principle we assembled genomes of the pigeon (Columbia livia) and peregrine falcon (Falco peregrinus) to chromosome level comparable, in continuity, to avian reference genomes. Both species are of interest for breeding, cultural, food and/or environmental reasons. Pigeon has a typical avian karyotype (2n=80) while falcon (2n=50) is highly rearranged compared to the avian ancestor. Using chromosome breakpoint data, we established that avian interchromosomal breakpoints appear in the regions of low density of conserved non-coding elements (CNEs) and that the chromosomal fission sites are further limited to long CNE “deserts”. This corresponds with fission being the rarest type of rearrangement in avian genome evolution. High-throughput multiple hybridization and rapid capture strategies using the current BAC set provide the basis for assembling numerous avian (and possibly other reptilian) species while the overall strategy for scaffold assembly and mapping provides the basis for an approach that could be applied to any animal genome