The ubiquitous RNA chaperone Hfq is involved in the regulation of key biological processes in many species across the bacterial kingdom. In the opportunistic human pathogen
Klebsiella pneumoniae
, deletion of the
hfq
gene affects the global transcriptome, virulence, and stress resistance; however, the ligands of the major RNA-binding protein in this species have remained elusive. In this study, we have combined transcriptomic, co-immunoprecipitation, and global RNA interactome analyses to compile an inventory of conserved and species-specific RNAs bound by Hfq and to monitor Hfq-mediated RNA–RNA interactions. In addition to dozens of RNA–RNA pairs, our study revealed an Hfq-dependent small regulatory RNA (sRNA), DinR, which is processed from the 3′ terminal portion of
dinI
mRNA. Transcription of
dinI
is controlled by the master regulator of the SOS response, LexA. As DinR accumulates in
K. pneumoniae
in response to DNA damage, the sRNA represses translation of the
ftsZ
transcript by occupation of the ribosome binding site. Ectopic overexpression of DinR causes depletion of
ftsZ
mRNA and inhibition of cell division, while deletion of
dinR
antagonizes cell elongation in the presence of DNA damage. Collectively, our work highlights the important role of RNA-based gene regulation in
K. pneumoniae
and uncovers the central role of DinR in LexA-controlled division inhibition during the SOS response.