Frequency-following and frequency-doubling neurons are ubiquitous in both striate and extrastriate visual areas. However, responses from these two types of neural populations have not been effectively compared in humans because previous EEG studies have not successfully dissociated responses from these populations. We devised a light–dark flicker stimulus that unambiguously distinguished these responses as reflected in the first and second harmonics in the steady-state visual evoked potentials. These harmonics revealed the spatial and functional segregation of frequency-following (the first harmonic) and frequency-doubling (the second harmonic) neural populations. Spatially, the first and second harmonics in steady-state visual evoked potentials exhibited divergent posterior scalp topographies for a broad range of EEG frequencies. The scalp maximum was medial for the first harmonic and contralateral for the second harmonic, a divergence not attributable to absolute response frequency. Functionally, voluntary visual–spatial attention strongly modulated the second harmonic but had negligible effects on the simultaneously elicited first harmonic. These dissociations suggest an intriguing possibility that frequency-following and frequency-doubling neural populations may contribute complementary functions to resolve the conflicting demands of attentional enhancement and signal fidelity—the frequency-doubling population may mediate substantial top–down signal modulation for attentional selection, whereas the frequency-following population may simultaneously preserve relatively undistorted sensory qualities regardless of the observer's cognitive state.