Sexually transmitted infections (STIs) in animals may have profound eco-evolutionary consequences, yet experimental studies of the sexual transmission of pathogens in wild populations are lacking. Here to identify sexually transmitted bacteria, we experimentally manipulated ejaculate transfer in black-legged kittiwakes (Rissa tridactyla) by blocking insemination after pairs had commenced copulating. We found that a Corynebacterium pathogenic strain was cleared from the cloaca of females five times more frequently in the experimental group, indicating it had been sexually transferred. A typical feature of STIs is that they reduce fertility, and in our kittiwake population, infected females suffered significantly higher hatching failure than uninfected females. Nevertheless, infected females achieved the same reproductive success as uninfected females by laying earlier and producing more eggs, suggesting reproductive compensation, a common strategy adopted by infected animals and plants. Our results provide new insights into the fitness consequences of STIs in a wild species and may stimulate further research on their evolutionary implications.