The mechanism by which light is converted into chemical energy in a natural photosynthetic system has drawn considerable research interest. Using fluorescence spectroscopy and microscopic imaging, we have observed fluctuating intermolecular protein fluorescence resonant energy transfers (FRET) among light-harvesting proteins I and II (LH1 and LH2) in bacterial photosynthetic membranes. Using two-channel, FRET, photon-counting detection and a novel, two-dimensional cross-correlation function amplitude-mapping analysis, we revealed fluorescence intensity and spectral fluctuations of donor (LH2) and acceptor (LH1) fluorescence involving FRET. Our results suggest that there are dynamic coupled and noncoupled states of the light-harvesting protein assemblies in photosynthetic membranes. The light-harvesting complex assembly under ambient conditions and under water involves dynamic intermolecular structural fluctuations that subsequently disturb the degree of energy transfer coupling between proteins in the membrane. Such intrinsic and dynamic heterogeneity of the native photosynthetic membranes, often submerged under the overall thermally induced spectral fluctuations and not observable in an ensemble-averaged measurement, likely plays a critical role in regulating the light-harvesting efficiency of the photosynthetic membranes.