The auditory oddball task is a well-studied stimulus paradigm used to investigate the neural correlates of simple target detection. It elicits several classic event-related potentials (ERPs), the most prominent being the P300 which is seen as a neural correlate of subjects’ detection of rare (target) stimuli. Though trial-averaging is typically used to identify and characterize such ERPs, their latency and amplitude can vary on a trial-to-trial basis reflecting variability in the underlying neural information processing. Here we simultaneously recorded EEG and fMRI during an auditory oddball task and identified cortical areas correlated with the trial-to-trial variability of task-discriminating EEG components. Unique to our approach is a linear multivariate method for identifying task-discriminating components within specific stimulus- or response-locked time windows. We find fMRI activations indicative of distinct processes that contribute to the single-trial variability during target detection. These regions are different from those found using standard, including trial-averaged, regressors. Of particular note is the strong activation of the lateral occipital complex (LOC). The LOC was not seen when using traditional event-related regressors. Though LOC is typically associated with visual/spatial attention, its activation in an auditory oddball task, where attention can wax and wane from trial to trial, indicates that it may be part of a more general attention network involved in allocating resources for target detection and decision making. Our results show that trial-to-trial variability in EEG components, acquired simultaneously with fMRI, can yield task-relevant BOLD activations that are otherwise unobservable using traditional fMRI analysis.