Many microbial taxa associated with healthy animals have both within-host and free-living populations, but little is known about the magnitude, persistence and dispersal of their populations in the external environment. Advances, particularly in our understanding of the population dynamics of free-living populations and microbial cycling between the external environment and hosts, can be achieved by the creative use of current technologies. In particular, there are opportunities to adapt methods, such as capture-mark-release techniques widely used in animal ecology, to the study of symbiotic microorganisms. Future technological advances are, however, required to monitor the location, proliferation and metabolic status at the scale of the single cell, especially under natural conditions. These advances will enable us to achieve precise quantification of host impacts on both micro-habitat suitability for microbial proliferation and microbial dispersal in the external environment. The resultant understanding of the fate of microorganisms shed from animal hosts is essential for the development of environmentally-safe and reliable microbial therapies for humans and animals of economic and environmental importance. Achieving an understanding of the ecology of symbiotic microorganisms is a key challenge for the discipline of environmental microbiology in the coming years.