The demographic history of dogs is complex, involving multiple bottlenecks, admixture events and artificial selection. However, existing genetic studies have not explored variance in the number of reproducing males and females, and whether it has changed across evolutionary time. While male-biased mating practices, such as male-biased migration and multiple paternity, have been observed in wolves, recent breeding practices could have led to female-biased mating patterns in breed dogs. For example, breed dogs are thought to have experienced a popular sire effect, where a small number of males father many offspring with a large number of females. Here we use genetic variation data to test how widespread sex-biased mating practices in canines are during different evolutionary time points. Using whole-genome sequence data from 33 dogs and wolves, we show that patterns of diversity on the X chromosome and autosomes are consistent with a higher number of reproducing males than females over ancient evolutionary history in both dogs and wolves, suggesting that mating practices did not change during early dog domestication. By contrast, since breed formation, we found evidence for a larger number of reproducing females than males in breed dogs, consistent with the popular sire effect. Our results confirm that canine demography has been complex, with opposing sex-biased processes occurring throughout their history. The signatures observed in genetic data are consistent with documented sex-biased mating practices in both the wild and domesticated populations, suggesting that these mating practices are pervasive.