Since at least the second Islamic century, Muslim ascetics-mystics (Sufis) regarded the Qur’an as a repository of profound esoteric-allegorical senses that are available only to the select few, especially those who have cleansed their hearts and souls of mundane attachments and aspirations, thereby rising above the crowd of ordinary believers. This approach to the scripture would often result in a drastic transformation of the exegete’s self through the process of deep meditation on the Qur’anic matrix of ideas and bringing them in resonance with his or her personal experiences, inclinations, and convictions. As a result of such esoteric-allegorical encounters of Muslim mystics with the Qur’an there has emerged a rich and sophisticated universe of meaning that could be used to confirm the validity of certain practices and spiritual and intellectual orientations that render Sufism distinct from other streams of Islamic thought and practice. By availing themselves of the Sufi universe of meaning and the exegetical tradition that supports Sufi teachers (shaykhs/murshids/pirs) came to lay claim to a super-rational, divinely-revealed and, eventually, salvific knowledge of God, the universe, and the human race. Their epistemological claims, in turn, have had long-ranging implications for the formation of Sufi institutions and their socio-political and ideological roles in Muslim societies. The paper examines the major stages in the formation of the body of esoteric-allegorical literature in Sufism from the eighth century CE until today, paying special attention to the remarkable stability of the topoi and methods employed by Sufi teachers to create a distinctive exegetical stream within Islam. It shows affinities and continuities between Sufi exegeses and those of the other esoteric traditions in Islam, especially Shi‘i and Isma‘ili ta’wil. After addressing the legitimacy of placing these distinctive movements onto the same analytic category (Islamic esotericism), as done, e.g., by Henri Corbin and his followers, the paper seeks to determine what exactly the knowledge claimed by these three traditions is all about and how it is related to the esoteric exegeses of medieval Christians and Jews and similar truth-claims and salvific promises based thereon.