The Deepwater Horizon (DWH) oil spill contaminated coastlines from Louisiana to Florida, burying oil up to 70 cm depth in sandy beaches, posing a potential threat to environmental and human health. The dry and nutrient-poor beach sand presents a taxing environment for microbial growth, raising the question how the biodegradation of the buried oil would proceed. Here we report the results of an in-situ experiment that (i) characterized the dominant microbial communities contained in sediment oil agglomerates (SOAs) of DWH oil buried in a North Florida sandy beach, (ii) elucidated the long-term succession of the microbial populations that developed in the SOAs, and (iii) revealed the coupling of SOA degradation to nitrogen fixation. Orders of magnitude higher bacterial abundances in SOAs compared to surrounding sands distinguished SOAs as hotspots of microbial growth. Blooms of bacterial taxa with a demonstrated potential for hydrocarbon degradation (Gammaproteobacteria, Alphaproteobacteria, Actinobacteria) developed in the SOAs, initiating a succession of microbial populations that mirrored the evolution of the petroleum hydrocarbons. Growth of nitrogen-fixing prokaryotes or diazotrophs (Rhizobiales and Frankiales), reflected in increased abundances of nitrogenase genes (nifH), catalyzed biodegradation of the nitrogen-poor petroleum hydrocarbons, emphasizing nitrogen fixation as a central mechanism facilitating the recovery of sandy beaches after oil contamination.