Over the last ten years, scholars have rediscovered the relevance of council democracy and workers’ councils for democratic thought. While these interventions are important, the literature lacks a coherent reconstruction of the development of council democracy in modern political thought. This article fills that lacuna by distinguishing between three conceptions of council democracy. One conception, advocated by Vladimir Lenin, interprets the councils as revolutionary organs able to destroy the old regime, but unable to govern afterwards. Another conception, favored by the interwar council communists, stresses the ability of workers’ councils to democratize the workplace, providing the germs of economic democracy. The third, delivered by Cornelius Castoriadis and Hannah Arendt, emphasizes the radical democratic nature of workers’ councils as an alternative to representative democracy. We argue that these three conceptions, notwithstanding their fundamental differences, share several core principles that can guide contemporary scholars to theorize the council as part of radical democratic repertoires. Moreover, we show the importance of these principles of council democracy for the constituent ambitions of contemporary movements like Occupy.