The effects of different monoterpenes and 2-cyclohexen-1-one on the antibacterial activity of nitrofurantoin against resistant Enterobacter cloacae, were compared and the minimal structural component of monoterpene required for the highest level of resistance-modulating activity was determined. Subinhibitory concentrations of all compounds tested enhanced the antibacterial activity of nitrofurantoin against E. cloacae to different extents. The highest synergistic effect was observed for the monoterpenes, like piperitone, which contained a conjugated ketone and C=C bond in their carbon ring structure. Piperitone also suppressed the emergence of nitrofurantoin-resistant strains of Enterobacteriaceae that were mutagenized by ethyl methanesulfonate. The modes of interaction of carvone, piperitone, and an enzyme inhibitor, benzoate, with nitroreductase were investigated by molecular docking and molecular dynamic (MD) simulation for 20 ns. MD simulation supported greater stability of the benzoate and monoterpene-nitroreductase (NR) complexes than of free NR. The results of this investigation are promising for the synthesis of more effective lead compounds to enhance the antibacterial activity of nitro drugs against resistant Enterobacter strains.