Inbreeding gives rise to continuous lengths of homozygous genotypes called runs of homozygosity (ROH) that occur when identical haplotypes are inherited from both parents. ROHs are enriched for deleterious recessive alleles and can therefore be linked to inbreeding depression, defined as decreased phenotypic performance of the animals. However, not all ROHs within a region are expected to have harmful effects on the trait of interest. We aimed to identify ROHs that unfavourably affect female fertility and milk production traits in the Finnish Ayrshire population. The estimated effect of ROHs with the highest statistical significance varied between parities from 9 to 17 days longer intervals from calving to first insemination, from 13 to 38 days longer intervals from first to last insemination and from 0.3 to 1.0 more insemination per conception. Similarly, for milk production traits ROHs were associated with a reduction of 208 kg for milk yield, 7 kg for protein yield and 16 kg for fat yield. We also found regions where ROHs displayed unfavourable effects across multiple traits. Our findings can be exploited for more efficient control of inbreeding depression, for example by minimizing the occurrence of unfavourable haplotypes as homozygous state in breeding programmes.