In many taxa, the left and right testes often differ in size. The compensation hypothesis states that one testis of the pair serves as a 'back-up' for any reduced function in the other and provides a mechanism to explain intraspecific variation in degree and direction of gonad asymmetry. Although testis asymmetry is common in birds, evidence for natural testis compensation is unknown. Using a novel quantitative approach that can be applied to any bilateral organ or structure, we show that testis compensation occurs naturally in birds and can be complete when one testis fails to develop. Owing to a recurrent risk of testis impairment and an evolutionary trade-off between natural and sexual selections acting on the arrangement of internal organs in species with abdominal and/or seasonal testes, compensation adds an important, but neglected, dimension to measures of male reproductive investment.