The history of human inbreeding is controversial. In particular, how the development of sedentary and/or agricultural societies may have influenced overall inbreeding levels is unclear. Here we present an approach for reliable estimation of runs of homozygosity (ROH) in genomes with ≥3x mean sequence coverage across >1 million SNPs, and apply this to 411 ancient Eurasian genomes from the last 15,000 years. We show that the frequency of inbreeding, as measured by ROH, has decreased over time. The strongest effect is associated with the Neolithic transition, but the trend has since continued, indicating a population size effect on inbreeding prevalence. We further show that most inbreeding in our historical sample can be attributed to small population size instead of consanguinity. We observed singular cases of high consanguinity only among members of farming societies.