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Abstract Brucella abortusis a facultative, intracellular, zoonotic pathogen that resides inside macrophages during infection. This is a specialized niche whereB. abortusencounters various stresses as it navigates through the macrophage. In order to survive this harsh environment,B. abortusutilizes post‐transcriptional regulation of gene expression through the use of small regulatory RNAs (sRNAs). Here, we characterize aBrucellasRNAs called MavR (forMurF‐andvirulence‐regulating sRNA), and we demonstrate that MavR is required for the full virulence ofB. abortusin macrophages and in a mouse model of chronic infection. Transcriptomic and proteomic studies revealed that a major regulatory target of MavR is MurF. MurF is an essential protein that catalyzes the final cytoplasmic step in peptidoglycan (PG) synthesis; however, we did not detect any differences in the amount or chemical composition of PG in the ΔmavRmutant. A 6‐nucleotide regulatory seed region within MavR was identified, and mutation of this seed region resulted in dysregulation of MurF production, as well as significant attenuation of infection in a mouse model. Overall, the present study underscores the importance of sRNA regulation in the physiology and virulence ofBrucella.