Refuse and promiscuous-landing synanthropic filth flies are transport hosts for a variety of viral, bacterial, and helminth pathogens of public health importance. Wild-caught non-biting flies associated with dairy cattle operations and animal and municipal waste processing sites were tested for transmissive stages of human enteric parasitic protozoans such as Cryptosporidium parvum oocysts, Giardia lamblia cysts, and spores of human-infectious microsporidia (i.e., Encephalitozoon intestinalis, E. hellem, E. cuniculi, and Enterocytozoon bieneusi) on their exoskeletons and in their digestive tracks. Oocysts and cysts have been identified by multiplexed Fluorescent In Situ Hybridization (FISH) combined with FITC-conjugated mAb, and microsporidian spores by FISH and PCR. At most of the sites, the quantities of C. parvum oocysts were positively correlated with the numbers of G. lamblia cysts, indicating a common source of contamination. More cysts occurred on exoskeletons than within the digestive tracts; this relationship was opposite for oocysts. Spores of E. bieneusi were identified for the first time from insect mechanical vectors; most of the spores were recovered from exoskeletons. The vast majority of oocysts, cysts, and spores were viable; 80, 69, and 87%, respectively. The biology and ecology of synanthropic filth flies suggest that their potential for mechanical transmission of human enteric parasites is high. As such, flies can acquire transmissive stages of human enteric parasites naturally from unhygienic sources and carry them on their surfaces and in their guts. They may be involved in the epidemiology of cryptosporidiosis, giardiasis, and microsporidiosis.