Serum response factor transcriptional activity is controlled through interactions with regulatory cofactors such as the coactivator MAL/MRTF‐A (myocardin‐related transcription factor A). MAL is itself regulated in vivo by changes in cellular actin dynamics, which alter its interaction with G‐actin. The G‐actin‐sensing mechanism of MAL/MRTF‐A resides in its N‐terminal domain, which consists of three tandem RPEL repeats. We describe the first molecular insights into RPEL function obtained from structures of two independent RPEL^MAL peptide:G‐actin complexes. Both RPEL peptides bind to the G‐actin hydrophobic cleft and to subdomain 3. These RPEL^MAL:G‐actin structures explain the sequence conservation defining the RPEL motif, including the invariant arginine. Characterisation of the RPEL^MAL:G‐actin interaction by fluorescence anisotropy and cell reporter‐based assays validates the significance of actin‐binding residues for proper MAL localisation and regulation in vivo. We identify important differences in G‐actin engagement between the two RPEL^MAL structures. Comparison with other actin‐binding proteins reveals an unexpected similarity to the vitamin‐D‐binding protein, extending the G‐actin‐binding protein repertoire.