Rab GTPases are the central regulators of intracellular traffic. Their function relies on their conformational change triggered by nucleotide exchange and hydrolysis. While this switch is well understood for an individual protein, how Rab GTPases collectively transition between different states is not known. Here, we combine in vitro reconstitution experiments with stochastic modelling to study the non-equilibrium properties of the minimal Rab5 activation network. We find that collective switching of Rab5 relies on a positive feedback and is triggered by intrinsic noise due to low amounts of Rab5[GDP] preexisting on the membrane. We show that this inactive population is not only the source of stochastic behavior of this biochemical circuit, but can act as a control parameter for Rab5 activation. We also discuss future directions regarding the effects of spatial constraints on stochastic switches in biological systems.