The ratio of male and female genetic map distances varies dramatically across the human genome. Despite these sex differences in genetic map distances, most multipoint linkage analyses use sex-averaged genetic maps. We investigated the impact of using a sex-averaged genetic map instead of sex-specific maps for multipoint linkage analysis of affected sibling pairs when identity-by-descent states are incompletely known due to missing parental genotypes and incomplete marker heterozygosity. If either all or no parental genotypes were available, for intermarker distances of 10, 5, and 1 cM, we found no important differences in the expected maximum lod score (EMLOD) or location estimates of the disease locus between analyses that used the sex-averaged map and those that used the true sex-specific maps for female:male genetic map distance ratios 1:10 and 10:1. However, when genotypes for only one parent were available and the recombination rate was higher in females, the EMLOD using the sex-averaged map was inflated compared to the sex-specific map analysis if only mothers were genotyped and deflated if only fathers were genotyped. The inflation of the lod score when only mothers were genotyped led to markedly increased false-positive rates in some cases. The opposite was true when the recombination rate was higher in males; the EMLOD was inflated if only fathers were genotyped, and deflated if only mothers were genotyped. While the effects of missing parental genotypes were mitigated for less extreme cases of missingness, our results suggest that when possible, sex-specific maps should be used in linkage analyses.