Despite advances in the neuroscience of visual consciousness over the last decades, we still lack a framework for understanding the scope of unconscious processing and how it relates to conscious experience. Previous research observed brain signatures of unconscious contents in visual cortex, but these have not been identified in a reliable manner, with low trial numbers and signal detection theoretic constraints not allowing to decisively discard conscious perception. Critically, the extent to which unconscious content is represented in high-level processing stages along the ventral visual stream and linked prefrontal areas remains unknown. Using a within-subject, high-precision, highly-sampled fMRI approach, we show that unconscious contents, even those associated with null sensitivity, can be reliably decoded from multivoxel patterns that are highly distributed along the ventral visual pathway and also involving prefrontal substrates. Notably, the neural representation in these areas generalised across conscious and unconscious visual processing states, placing constraints on prior findings that fronto-parietal substrates support the representation of conscious contents and suggesting revisions to models of consciousness such as the neuronal global workspace. We then provide a computational model simulation of visual information processing/representation in the absence of perceptual sensitivity by using feedforward convolutional neural networks trained to perform a similar visual task to the human observers. The work provides a novel framework for pinpointing the neural representation of unconscious knowledge across different task domains.