Zayn al-Din Khwafi (d. 1435), a prominent mystic of the fifteenth century, is the author of numerous treatises on Sufism. Many of his works found wide reception in his lifetime and some even continued to be copied until the nineteenth century. One work—namely, Manhaj al-Rashad—stands out among the rest not only in its very limited circulation but also in that it attracted the most scholarly attention. Recent studies on the religious history of the Timurid and the Ottoman worlds have highlighted the importance of Manhaj al-Rashad for the intellectual controversies of the mid-fifteenth century, drawing attention to how Khwafi’s perspective on Ibn Arabi was indicative of the polarized milieu of the mystics of the time. Building on this scholarship, I present in this paper a detailed study of the Manhaj with the goal of situating it in a meaningful context of mystical writing that emerged with the eleventh century authors including Abu Hamid al-Ghazali (d. 1111), the author of Al-Munqid min al-Dalal. In agreement with these recent studies, I argue that the rightful historical context for the compilation of this work is the chaotic political climate of Shahrukh’s (d. 1447) reign in Herat. However, a deeper understanding is possible only when the work is read against the backdrop of a tradition of Sufi apologetics, which Khwafi unambiguously refers to. This comparative analysis of Manhaj al-Rashad reveals its author as an inheritor of the kind of Sufi intellectual al-Ghazali had been for his time and milieu. What emerges from this examination is the figure of a tariqa-founding Khwafi as the commanding Sufi of the Timurid capital, championing the historic tradition of shari’a-minded Sufism. I argue that one remarkable difference between the two apologies—namely al-Munqid and the Manhaj—was Khwafi’s strong defense of Shahrukh, obedience to whom he understood as the religious duty of all.