Teleost fish are one of the most species-rich and diverse clades amongst vertebrates, which makes them an outstanding model group for evolutionary, ecological and functional genomics. Yet, despite a growing number of sequence reference genomes, large-scale comparative analysis remains challenging in teleosts due to the specifics of their genomic organization. As legacy of a whole genome duplication dated 320 million years ago, a large fraction of teleost genomes remain in duplicate paralogous copies. This ancestral polyploidy confounds the detailed identification of orthologous genomic regions across teleost species. Here, we combine tailored gene phylogeny methodology together with the state-of-the art ancestral karyotype reconstruction to establish the first high resolution comparative atlas of paleopolyploid regions across 74 teleost fish genomes. We show that this atlas represents a unique, robust and reliable resource for fish genomics. We then use the comparative atlas to study the tetraploidization and rediploidization mechanisms that affected the ancestor of teleosts. Although the polyploid history of teleost genomes appears complex, we uncover that meiotic recombination persisted between duplicated chromosomes for over 60 million years after polyploidization, suggesting that the teleost ancestor was an autotetraploid.