Transcription by RNA polymerases (RNAPs) is essential for cellular life. Genes are often transcribed by multiple RNAPs. While the properties of individual RNAPs are well appreciated, it remains less explored whether group behaviors can emerge from co-transcribing RNAPs under most physiological levels of gene expression. Here, we provide evidence in Escherichia coli that well-separated RNAPs can exhibit collaborative and antagonistic group dynamics. Co-transcribing RNAPs translocate faster than a single RNAP, but the density of RNAPs has no significant effect on their average speed. When a promoter is inactivated, RNAPs that are far downstream from the promoter slow down and experience premature dissociation, but only in the presence of other co-transcribing RNAPs. These group behaviors depend on transcription-induced DNA supercoiling, which can also mediate inhibitory dynamics between RNAPs from neighboring divergent genes. Our findings suggest that transcription on topologically-constrained DNA, a norm across organisms, can provide an intrinsic mechanism for modulating the speed and processivity of RNAPs over long distances according to the promoter’s on/off state.