Microbial populations often rely on the cooperative production of extracellular public goods molecules. The cooperative nature of public good production may lead to minimum viable population sizes, below which populations collapse. In addition, cooperator public goods producing cells face evolutionary competition from non-producing mutants, or freeloaders. Thus, public goods cooperators have to be stable not only to the invasion of freeloaders, but also to ecological perturbations that may push their numbers too small to be sustainable. Through a combination of experiments with microbial populations and mathematical analysis of the Ecological Public Goods Game, we show that game parameters and experimental conditions that improve the evolutionary stability of cooperators also lead to a low ecological stability of the cooperator population. Complex regulatory strategies mimicking those used by microbes in nature may allow cooperators to beat this eco-evolutionary stability tradeoff and become resistant to freeloaders while at the same time maximizing their ecological stability. Our results thus identify the coupled eco-evolutionary stability as being key for the long-term viability of microbial public goods cooperators.