When cuckoldry is frequent we can expect fathers to withhold investment in offspring that may not be theirs. Human paternal investment can be substantial and is in line with observations from tens of thousands of conceptions that suggest that cuckoldry is rare in humans. The generality of this claim seems to be in question as the rate of cuckoldry varies across populations and studies have mostly been on Western populations. Two additional factors complicate our conclusions, (1) current estimates of the rate of cuckoldry in humans may not reflect our past behaviour as adultery can be concealed by the use of contraceptives; and (2) it is difficult to obtain samples that are random with respect to their paternity certainty. Studies that combine genealogies with Y-chromosome haplotyping are able to circumvent some of these problems by probing into humans’ historical behaviour. Here we use this approach to investigate 1273 conceptions over a period of 330 years in 23 families of the Afrikaner population in South Africa. We use haplotype frequency and diversity and coalescent simulations to show that the male population did not undergo a severe bottleneck and that paternity exclusion rates are high for this population. The rate of cuckoldry in this Western population was 0.9% (95% confidence interval 0.4–1.5%), and we argue that given the current data on historical populations we have to conclude that, at least for Western human populations, cuckoldry rate is probably in the range of 1%.