Visual imagery and veridical perception are phenomenologically related, suggesting that they share neural machinery. Previous research confirmed this assumption at the macroscale of human cortical organization in category-selective regions in ventral visual cortex. However, imagery and perception differ fundamentally in the information flow that underlies them: perception is driven by the integration of sensory feedforward and internally-generated feedback information, whereas imagery depends on feedback only. This suggests that while visual imagery and perception may activate common cortical regions, they do so in fundamentally distinctive ways. To investigate, we resolved neural activity during imagery and perception in the ventral visual cortex at the level of laminar organization that anatomically and functionally distinguishes feedforward from feedback information flow. We found distinctive laminar profiles for imagery and perception of scenes and faces in parahippocampal place area (PPA) and fusiform face area (FFA) respectively. Our findings clarify the neural basis of the phenomenology of visual imagery versus perception, and shed new light on how feedforward and feedback information processing in high-level ventral visual cortex orchestrates human object vision.