Recent neuropsychological and imaging data have implicated different brain networks in the processing of different word classes, nouns being linked primarily to posterior, visual object-processing regions and verbs to frontal, motor-processing areas. However, as most of these studies have examined words in isolation, the consequences of such anatomically based representational differences, if any, for the processing of these items in sentences remains unclear. Additionally, in some languages many words (e.g. `drink’) are class-ambiguous, i.e. they can play either role depending on context, and it is not yet known how the brain stores and uses information associated with such lexical items in context. We examined these issues by recording event-related potentials (ERPs) in response to unambiguous nouns (e.g. `beer’), unambiguous verbs (e.g. `eat’), class-ambiguous words and pseudowords used as nouns or verbs within two types of minimally contrastive sentence contexts: noun-predicting (e.g. `John wanted THE [target] but …’) and verb-predicting (`John wanted TO [target] but …’). Our results indicate that the nature of neural processing for nouns and verbs is a function of both the type of stimulus and the role it is playing. Even when the context completely specifies their role, word class-ambiguous items differ from unambiguous ones over frontal regions by ~150 ms. Moreover, whereas pseudowords elicit larger N400s when used as verbs than when used as nouns, unambiguous nouns and ambiguous words used as nouns elicit more frontocentral negativity than unambiguous verbs and ambiguous words used as verbs, respectively. Additionally, unambiguous verbs elicit a left-lateralized, anterior positivity (~200 ms) not observed for any other stimulus type, though only when these items are used appropriately as verbs (i.e. in verb-predicting contexts). In summary, the pattern of neural activity observed in response to lexical items depends on their general probability of being a verb or a noun and on the particular role they are playing in any given sentence. This implicates more than a simple two-way distinction of the brain networks involved in their storage and processing. Experience, as well as context during on-line language processing, clearly shapes the neural representations of nouns and verbs, such that there is no single neural marker of word class. Our results further suggest that the presence and nature of the word class-based dissociations observed after brain damage are similarly likely to be a function of both the type of stimulus and the context in which it occurs, and thus must be assessed accordingly.