The incidence of extra-pair paternity (EPP) is highly variable across bird taxa. While EPP is known to affect reproductive variance, the causes of temporal variation in rates of EPP are poorly studied. Breeding density has often been proposed as an important factor influencing EPP variation, but it has received mixed support. Over a 5-year period we examined the rate of EPP in a socially monogamous Grasshopper Sparrow (Ammodramus savannarum) population on a restored grassland in Maryland. Of 124 broods, 62.1% had extra-pair young (EPY), and of 448 nestlings, 36.8% were the result of extra-pair fertilizations. Over the 5-year study, percent EPY ranged from 26% to 60%. EPP rates were positively correlated with the local density of territorial males, supporting the density hypothesis, and 81% of the EPY were from neighboring males. Male within-pair mating success was related to extra-pair mating, suggesting an active behavioral tradeoff between within- and extra-pair matings, especially at high densities. By examining males at the individual level, we found males that were not cuckolded also had the most genetic offspring (within-pair and extra-pair), whereas males that were cuckolded also failed to sire many extra-pair offspring. Here we show that density plays an important role in the availability of mates, EPP, and the opportunity for sexual selection. Received 9 April 2016. Accepted 3 August 2017.