Hydrocarbon contaminants in groundwater can be degraded by microbes under different redox settings, forming hot spots of degradation especially at the fringes of contaminant plumes. At a tar-oil-contaminated aquifer in Germany, it was previously shown that the distribution of anaerobic toluene degraders as traced via catabolic and ribosomal marker genes is highly correlated to zones of increased anaerobic degradation at the lower fringe of the plume. Here, we trace the respective distribution of aerobic toluene degraders over a fine-scale depth transect of sediments taken at the upper fringe of the plume and below, based on the analysis of 16S rRNA genes as well as catabolic markers in intervals of 3–10 cm. Well-defined small-scale distribution maxima of typical aerobic degrader lineages within the Pseudomonadaceae, Comamonadaceae and Burkholderiaceae are revealed over the redox gradient. An unexpected maximal abundance of 9.2 × 106 toluene monooxygenase (tmoA) genes per g of sediment was detected in the strongly reduced plume core, and gene counts did not increase towards the more oxidized upper plume fringe. This may point towards unusual ecological controls of these yet unidentified aerobic degraders, and indicates that competitive niche partitioning between aerobic and anaerobic hydrocarbon degraders in the field is not yet fully understood. These findings demonstrate the potential of catabolic marker gene assays in elaborating the ecology of contaminant plumes, which is a prerequisite for developing integrated monitoring strategies for natural attenuation.