Understanding the behavioural mechanisms that mediate pathogen transmission in social hosts like birds could provide the empirical bases for explaining the epidemiological dynamics of zoonotic infections in vertebrates. By experimentally infecting the feathers and cloaca of captive zebra finches (Taeniopygia guttata), with the bacterium Bacillus licheniformis PWD1 (BL), we examined the self-contamination and horizontal transmission of birds sharing the same environment. We also examined whether sexual transmission of bacteria is gender biased. Our results show that bacteria placed on the plumage of the birds lead to self and allo-infections of the bird guts, possibly through preening behaviours and bacterial ingestion. Furthermore, we found that sexual transmission of the bacteria was asymmetrical, being higher when males are the transmitting sex. Our results suggest the existence of an oral-faecal-genital route of bacterial transmission for avian hosts, wherein bacteria present on feathers infect their host guts through self and allo-preening and bacterial ingestion. Gut bacteria can then be transmitted sexually with transmission rate being higher when males are the infected sex.