Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.