Studies of a handful of species reveal two mechanisms by which meiotic recombination is directed to the genome - through PRDM9 binding or by targeting promoter-like features - that lead to dramatically different evolutionary dynamics of hotspots. Here, we identified PRDM9 from genome and transcriptome data in 225 species, finding the complete PRDM9 ortholog across distantly related vertebrates. Yet, despite its broad conservation, we inferred a minimum of six partial and three complete losses. Strikingly, taxa carrying the complete ortholog of PRDM9 are precisely those with rapid evolution of its predicted binding affinity, suggesting that all its domains are necessary for directing recombination. Indeed, as we show, swordtail fish carrying a partial ortholog share recombination properties with PRDM9 knock-outs.