While the P3 component during target detection and novelty processing has been widely studied, less is known about its underlying network dynamics. A recent cognitive model suggests that frontal‐parietal and frontal‐temporal interregional connectivity are related to attention/action selection and target‐related memory updating during the P3, respectively, but empirical work testing this model is lacking. Other work suggests the importance of theta‐ and delta‐band connectivity between the medial frontal cortex and distributed cortical regions during attention, stimulus detection, and response selection processes, and similar dynamics may underlie P3‐related network connectivity. The present study evaluated the functional connectivity elicited during a visual task, which combined oddball target and novelty stimuli, in a sample of 231 same‐sex twins. It was hypothesized that both target and novel conditions would involve theta frontoparietal connectivity and medial frontal theta power, but that target stimuli would elicit the strongest frontotemporal connectivity. EEG time‐frequency analysis revealed greater theta‐band frontoparietal connectivity and medial frontal power during both target and novel conditions compared to standards, which may index conflict/uncertainty resolution processes. Theta‐band frontotemporal connectivity was maximal during the target condition, potentially reflecting context updating or stimulus‐response activation. Delta‐band frontocentral‐parietal connectivity was also strongest following targets, which may be sensitive to response‐related demands. These results suggest the existence of functional networks related to P3 that are differentially engaged by target oddballs and novel distractors. Compared to simple P3 amplitude, network measures may provide a more nuanced view of the neural dynamics during target detection/novelty processing in normative and pathological populations.