Mammalian karyotypes vary wildly in haploid number (e.g., 3-40 in deer) compared to stability in teleost fish (24-25 in 58% of teleosts), but we don’t understand the mechanisms that account for differences in karyotype stability. Among perciform teleosts, platyfish (Xiphophorus maculatus) and medaka (Oryzias latipes) both have 24 chromosome pairs but threespine stickleback (Gasterosteus aculeatus) and green pufferfish (Tetraodon nigroviridis) have just 21 pairs. What mechanisms reduced chromosome number? Under one hypothesis, six ancestral chromosomes fused in pairs to make three chromosomes. Alternatively, four ancestral chromosomes might have fused to make a single large derived chromosome. More complicated hypotheses are also possible. Furthermore, chromosome fusions could be shared or lineage specific. To distinguish among hypotheses, we made a meiotic map for platyfish with over 16,000 mapped markers. Along the map we tiled genomic contigs, and compared genomes using the Synteny Database. Analysis showed that chromosomes of platyfish and medaka (both Atherinomorpha within Percomorpha) remained remarkably unchanged by translocation, but experienced numerous transpositions and inversions since their lineages diverged about 120 million years ago. In contrast, reduced chromosome numbers in other Percomorpha groups (stickleback (Gasterosteidae) and green pufferfish (Tetraodontoformes)) arose by fusion of pairs of ancestral chromosomes after their lineage diverged from platyfish about 195 million years ago. These studies reveal stability of syntenies and gene orders in teleost chromosomes over hundreds of millions of years, identify what are likely genome assembly errors, characterize chromosome fusion events, and distinguish independent chromosome fusions.