In this paper, we explore the way the evolution of entrepreneurial ecosystems is shaped by different governance designs. We propose a theoretical framework in which we discuss what type of governance design would best fit the needs of an entrepreneurial ecosystem throughout its evolution. We also provide argumentations concerning the mechanisms that may explain the evolution through the different governance configurations. The conceptualization of a new framework has allowed us to specify a set of propositions, which we have tested on one single empirical setting, represented by Turin’s entrepreneurial ecosystem. The paper introduces some important policy implications. It highlights the need for a more complex relational form of governance for the growth of an entrepreneurial ecosystem, which could be obtained by means of a systemic and participative approach rooted in shared cooperative norms and informal routines.