This article explores Milton’s engagement with his biblical model for the epic genre throughout his diffuse epic. Paradise Lost draws from Job in its depictions of the wonder of creation, the agony of despair, and the boldness of a creature to question the creator. While some Renaissance commentators find the combativeness of Job’s complaint to be theologically problematic, Milton infuses it into his depictions of the unfallen Adam and the Son who exercise the digestive functions of reason in their freedom to debate with God. These Joban echoes demonstrate that hubristic presumption directed toward dialogue with the creator is characteristic of the righteous; it is the rigidity of despair that avoids such dialogue and leads to the Fall. In the end, through a network of carefully placed allusions to the scriptural epic of suffering, Milton achieves a model of righteous questioning as a safeguard against error and despair.