Farming cooperatives are organisations fundamentally based on social capital. However, the neoliberal and globalisation turn in the food system have led to the economisation of agricultural cooperatives as their main objective and criteria for evaluating their performance, and to a retreat from their participation in the wider cooperative movement. Nevertheless, new models of cooperation may provide a method to divert from this neoliberalisation trend by promoting social capital and mutual learning amongst different actors committed to a transition to sustainable food systems. This paper applies the anthropological concept of third spaces to examine the case of multistakeholder cooperatives. This type of food and farming cooperatives are composed of a diverse membership groups (e.g., producers, consumers, coordinators, buyers, etc). A nuanced analysis of these cooperatives’ capacity to generate social capital, and more specifically to blur the boundaries between bonding, bridging, and linking social capital, is presented. Evidence from five case studies suggests that multistakeholder cooperatives that remain at the border of their game, operating in both real and symbolic third spaces, are more likely to be based on and reproduce different types of social capital as well as social and environmental sustainability, while in turn reducing the risk of co-optation of their transformative practices.