Directional asymmetry in gonad size is commonly observed in vertebrates and is particularly pronounced in birds, where the left testis is frequently larger than the right. The adaptive significance of directional asymmetry in testis size is poorly understood, and whether it extends beyond the testes (i.e. side-correspondent asymmetry along the reproductive tract) has rarely been considered. Using the Maluridae, a songbird family exhibiting variation in levels of sperm competition and directional testis asymmetry, yet similar in ecology and life history, we investigated the relative roles of side-correspondence and sperm competition on male reproductive tract asymmetry at both inter- and intraspecific levels. We found some evidence for side-correspondent asymmetry. Additionally, sperm competition influenced directional asymmetry at each end of the reproductive tract: species experiencing higher levels of sperm competition had a relatively larger right testis and relatively more sperm in the right seminal glomerus. Within red-backed fairy-wrens (Malurus melanocephalus), auxiliary males had relatively more sperm in the left seminal glomerus, in contrast to a right-bias asymmetry throughout the reproductive tract in breeding males. Given that the number of sperm is important for competitive fertilization success, our results suggest that sperm competition shapes reproductive asymmetries beyond testis size, with likely functional consequences for male reproductive success. peerReviewed