This paper argues that a new civil society is emerging in Israel that is fundamentally distinct from the old state-led civil society. Its core organising logic is cosmopolitan, universalist and post-Zionist, expanding its sphere of contestation to challenge the ethno-nationalist and communitarian basis of the enduring Zionist societal consensus. The implications of this phenomenon are uniquely profound for the Israeli context. A cosmopolitan post-Zionist civil society challenges the raison d'être of the state in its current ethno-nationalist construction, calling for the inclusion of marginalised groups into its sphere. The Jewish people have for long debated the merits of universalist ethics vis-à-vis particularistic considerations. The horrors of the Holocaust tilted the balance of the debate in favour of the communitarians, culminating with the establishment of the state of Israel as a Jewish national home. More recently, a growing interconnectedness of social relations has forced a reassessment of the moral basis of the Israeli society reigniting once again the rift, this time between Zionist communitarians and post-Zionist cosmopolitans. To develop this argument, the old and the new civil society will be contrasted on the basis of the conceptual limitations of common understandings of civil society. This will enable an adequate assessment of the empirical and aspirational forms of the term and the merits of a cosmopolitan post-Zionist civil society in a global age. The emerging phenomenon will be then explained through the ongoing process of displacement of identities which have forced Israelis to reconsider existing perceptions of the self, the meaning of being an Israeli; and the construction of external others. Finally, it will be concluded that Israel is at a cross-roads and civil society can play a key role in drawing the future of the state.