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Genetic triggers for sex determination are frequently co-inherited with other linked genes that may also influence one or more sex-specific phenotypes. To better understand how sex-limited regions evolve and function, we studied a small W chromosome-specific region of the frogXenopus laevisthat contains only three genes (dm-w,scan-w,ccdc69-w) and that drives female differentiation. Using gene editing, we found that the sex-determining function of this region requiresdm-wbut thatscan-wandccdc69-ware not essential for viability, female development, or fertility. Analysis of mesonephros+gonad transcriptomes during sexual differentiation illustrates masculinization of thedm-wknockout transcriptome, and identifies mostly non-overlapping sets of differentially expressed genes in separate knockout lines for each of these three W-specific gene compared to wildtype sisters. Capture sequencing of almost allXenopusspecies and PCR surveys indicate that the female-determining function ofdm-wis present in only a subset of species that carry this gene. These findings map out a dynamic evolutionary history of a newly evolved W chromosome-specific genomic region, whose components have distinctive functions that frequently degraded duringXenopusdiversification, and evidence the evolutionary consequences of recombination suppression.