Gene and genome duplications serve as an important reservoir of material for the evolution of new biological functions. It is generally accepted that many genes present in vertebrate genomes owe their origin to two whole genome duplications that occurred deep in the ancestry of the vertebrate lineage. However, details regarding the timing and outcome of these duplications are not well resolved. We present high-density meiotic and comparative genomic maps for the sea lamprey, a representative of an ancient lineage that diverged from all other vertebrates approximately 550 million years ago. Linkage analyses yielded a total of 95 linkage groups, similar to the estimated number of germline chromosomes (1N ~ 99), spanning a total of 5,570.25 cM. Comparative mapping data yield strong support for one ancient whole genome duplication but do not strongly support a hypothetical second event. Rather, these comparative maps reveal several evolutionary independent segmental duplications occurring over the last 600+ million years of chordate evolution. This refined history of vertebrate genome duplication should permit more precise investigations into the evolution of vertebrate gene functions.