This study seeks to explore the incentive factors that serve to instigate university engagement in the third-mission agenda based on evidence drawn from the Russian system of higher education. We pay special attention to how the split of natural and externally induced drivers of the third mission has changed from the Soviet era and up until the immediate modernity. Our analysis has shown that the balance of these two types of incentives never remained flat over the course of history as the Russian university system encountered and had to address different challenges and imperatives at various points in time. We have also found that, while federal initiatives have been adopted by the Russian state that have created a distinctive cohort of universities entrusted with comprehensively contributing to the socio-economic and innovative potential of their host localities as a top-priority task, the third-mission agenda is by no means reduced solely to this very group of institutions, as there are many other universities that are not directly expected to focus on the third mission, but which still favor pursuing proactive and fruitful collaborations with regional stakeholders as arguably representing one of the crucial factors in long-term university sustainability.