Insight into complex evolutionary histories continues to build through broad comparative phylogenomic and population genomic studies. We assay thousands of nuclear ddRADseq loci, including Z sex chromosome and autosomal linked loci for 363 specimens to investigate the evolutionary history of the Mergini tribe (sea ducks). We couple multi-species comparisons with phylogenomic analyses, and show that the species are strongly structured across all sampled marker types, with clear genetic assignments of individuals to their respective species, and phylogenetic relationships recapitulate known relationships. Despite strong species integrity, we identify at least 18 putative hybrids with all but one being late generational backcrosses. Most interesting, we provide the first evidence that an ancestral gene flow event between long tailed-ducks and true Eiders resulted in the movement of genetic material into the former species, and likely generated a novel species - the Steller's eider - via hybrid speciation. Despite generally low contemporary levels of gene flow, we conclude that hybridization has and continues to be an important process that shifts novel genetic variation between species within the tribe Mergini.