While “conservative” political philosophy in Iran has often been read as closely aligned with the state’s ideological orientation, philosophers associated with the “critical rationalist school” (aql girai-i intiqadi), represent the regime’s most enduring and trenchant critics. An exemplary figure from this movement is the contemporary theologian and philosopher Abdolkarim Soroush (b. 1945). Soroush has famously critiqued Ayatollah Khomeini’s theory of “Guardianship of the Jurisconsult” as epistemologically naïve and incompatible with a historical-critical reading of Islamic sacred sources. According to Heydar Shadi, Soroush’s early and mid-career writings are largely responsible for the “epistemic turn” in contemporary Iranian discourse. What has triggered strong reactions from conservative and traditionalist thinkers has been Soroush’s assertion that the Prophet Muhammad played a major role in shaping the form and content of the Qur’an—a stance which Behrooz Ghamari-Tabrizi has described as walking the line of heterodoxy and blasphemy in Muslim theological circles. More recently, Soroush’s Muhammad’s Word, Muhammad’s Dream (2018) adds new sophistication (as well as critical ambiguities) to Soroush’s “humanistic” account of prophecy. This paper constructs a genealogy of Soroush’s anti-establishment thinking on prophecy, Islamic governance, and political theory. In contending, in Muhammad’s Word, that many passages of the Qur’an are best understood as Muhammad’s historically situated accounts of dreams and visions (ru’ya), Soroush deepens his critique of the political and legal assumptions of the Islamic Republic’s constitutional foundation. In elucidating this dynamic, I juxtapose a decontextual view of the legal and regulatory content of the Qur’an—endorsed by many regime defenders—with Soroush’s historicizing project, which views all such scriptural passages as time-bound and subject to revision. Such a radical appraisal is made possible by Soroush’s invocation of “counterfactual” reasoning about the form and content of the Qur’anic text: if differing historical circumstances would have affected the cause (‘illa) behind a given Qur’anic injunction, then such legal content should not be seen as essential to the text. Moreover, in Muhammad’s Word, Soroush continues to press his fallibilism about religious knowledge, which undermines the Iranian regime’s claim to possess an “official reading” of the canonical sources of Islamic law and political theory. In sum, this paper constructs an overall trajectory of Soroush’s regime-critical scholarship and highlights the emphasis on prophecy as an animating force of Soroush’s most recent political-philosophical critiques.