In sexually reproducing taxa, normal sperm function is critical for successful reproduction, and pathogenic bacteria can prevent this. Thus, understanding the role of bacteria in ejaculates can have significant implications for ecology and evolution. Although a few studies have investigated the human ejaculate microbiota, the amount of culture-independent research on other species is limited. By utilizing high-throughput sequencing of 16S rRNA gene amplicons, significant advances can be made in the knowledge of diverse bacterial communities. This study describes and compares the ejaculate microbiota of the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and Italian sparrow (P. italiae). These species constitute a hybrid species system in which the Italian sparrow originated through hybridization between the house and Spanish sparrow, and occur in both allo- and sympatry throughout Europe. I found the composition and structure of the sparrow ejaculate microbiota to be highly variable between individuals, and this obscured any species-specific signal. Individuals at different locations did however trend towards being different. I detected a wide range of bacteria belonging to 36 phylum-level classifications, of which Bacteroidetes and Proteobacteria were the most abundant. At the genus level, I found Flavobacterium to dominate the avian ejaculate microbiota. Notably, a considerable variety of bacteria classified to unculturable candidate phyla were detected. Overall, I found large overlap with taxa commonly found in the avian gastrointestinal tract and human ejaculate, as well as with previous culture-based studies on avian ejaculate. A wide range of potential pathogens likely to detriment host health or sperm function were detected. It is likely that these cause similar selective pressures on the mating systems in the three species, as no species-specific microbiota is detected. This study presents a significant advance in knowledge on the composition and structure of the avian ejaculate microbiota.