Language comprehension involves multiple hierarchical processing stages across time, space, and levels of representation. When processing a word, the sensory input is transformed into increasingly abstract representations that need to be integrated with the linguistic context. Thus, language comprehension involves both input-driven as well as memory-dependent processes. While neuroimaging research has identified the most important time windows and brain regions implicated in these processes, recent studies indicate that whole-brain distributed patterns of cortical activation might be highly relevant for cognitive functions, including language. One such pattern, based on resting-state connectivity, is the ‘principal cortical gradient’, which dissociates sensory from heteromodal brain regions. The present study investigated the extent to which this gradient provides an organizational principle underlying language function, using a multimodal neuroimaging dataset of functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) recordings from 102 participants during sentence reading. We found that individual representations of a word (word length, orthographic distance and word frequency), which reflect visual, orthographic, and lexical properties, are mainly represented at the sensory end of the gradient. Although these properties showed opposite effect directions in fMRI and MEG, their association to the sensory end of the gradient was consistent across both neuroimaging modalities. In contrast, MEG revealed that properties reflecting a word’s relation to its linguistic context (semantic similarity and position within the sentence) predominantly involve the heteromodal end of the gradient. This dissociation between individual word and contextual properties was stable across earlier and later time windows during word presentation, indicating interactive processing of word representations and linguistic context at opposing ends of the principal gradient. To conclude, our findings indicate that the principal gradient underlies the organization of a range of linguistic representations while supporting a distinction between context-independent and context-dependent representations. Furthermore, the gradient reveals convergent patterns across neuroimaging modalities (similar location along the gradient) in the presence of divergent responses (opposite effect directions).