The transcriptional activator FlhD 2C 2 is the master regulator of bacterial flagellum biogenesis and swarming migration, activating the “early” class II promoters of the large flagellar gene hierarchy. Using primer extensions, band-shift assays, and enzymatic and chemical footprinting, we describe the binding of the FlhD 2C 2 heterotetramer to the promoter regions of four class II flagella operons, fliAZ, flhBA and the divergent flgAMN and flgBCD(EFGHIJ). Each of the promoter regions was bound by a single heterotetramer, i.e. the flgAMN and flgBCD operons are characterised by a single FlhD 2C 2 binding site. Binding affinity differed, and correlated with previously reported promoter strength and order of activation. Methylation protection and interference, and depurination and depyrimidation interference provided a detailed map of critical bases within a common 46–59 bp DNaseI footprint overlapping the promoter −35 sequences. These data and compilation of the 12 known class II promoter sequences of Escherichia coli, Proteus mirabilis and Salmonella typhimurium allowed determination of a FlhD 2C 2 binding site with pseudo symmetry, comprising two 17–18 bp inverted repeats, each a consensus FlhD 2C 2 box, separated by a 10–11 bp spacer. DNaseI hypersensitivity indicated that binding may cause a conformational change in the promoter regions. Only the FlhC subunit can bind DNA independently, but the specificity and stability of the interaction is strengthened by FlhD. Here, photo-crosslinking established that both FlhC and the stabilising FlhD contact the DNA within the FlhD 2C 2 tetramer. Our data suggest that specificity of recognition and stability of the FlhD 2C 2/DNA complex require protein–protein interaction and interaction of both FlhC and FlhD subunits with DNA. These characteristics of the FlhD and FlhC subunits in the FlhD 2C 2/DNA complex are strikingly atypical of prokaryotic regulators.