Cheating in microbial communities is often regarded as a precursor to a “tragedy of the commons”, ultimately leading to over-exploitation by a few species, and destabilisation of the community. However, this view does not explain the ubiquity of cheaters in nature. Indeed, existing evidence suggests that cheaters are not only evolutionarily and ecologically inevitable, but also play important roles in communities, like promoting cooperative behaviour. We developed a chemostat model with two microbial species and a single, complex nutrient substrate. One of the organisms, an enzyme producer, degrades the substrate, releasing an essential and limiting resource that it can use both to grow and produce more enzymes, but at a cost. The second organism, a cheater, does not produce the enzyme but benefits from the diffused resource produced by the other species, allowing it to benefit from the public good, without contributing to it. We investigated evolutionarily stable states of coexistence between the two organisms and described how enzyme production rates and resource diffusion influence organism abundances. We found that, in the long-term evolutionary scale, monocultures of the producer drive themselves extinct because selection always favours mutant invaders that invest less in enzyme production. However, the presence of a cheater buffers this runaway selection process, preventing extinction of the producer and allowing coexistence. Resource diffusion rate controls cheater growth, preventing it from outcompeting the producer. These results show that competition from cheaters can force producers to maintain adequate enzyme production to sustain both itself and the cheater. This is known in evolutionary game theory as a “snowdrift game” – a metaphor describing a snow shoveler and a cheater following in their clean tracks. We move further to show that cheating can stabilise communities and possibly be a precursor to cooperation, rather than extinction.