The high acuity of hearing in mammals requires an active mechanical process boosting vibration in the inner ear. ‘Cochlear amplification’ is provided by high-frequency cellular motility of auditory outer cells (OHCs). This ‘electromotility’ is generated by prestin (SLC26A5), an OHC-specific membrane protein acting as an electro-mechanical transducer. Intriguingly, Prestin belongs to the SLC26/SulP family of anion transporters that mediate the translocation of inorganic and small organic anions.Biophysically, prestin acts as an area motor by alternating between two conformations that occupy different cross-sectional areas within the membrane. Joint conformational transitions of the tightly packed prestin motors in the plasma membrane of the OHC are driven by changes in membrane potential and result in macroscopic cellular length changes. The molecular mechanism underlying electromotility is probably related to the ion transport cycle in SLC26 transporters, as non-mammalian prestin orthologs are anion antiporters and prestin-driven electromotility is strictly anion-dependent. Beyond these observations, however, the molecular mechanisms underlying motor activity and transport by SLC26 proteins remained essentially unknown, as structural information for the SulP transporter family is lacking. We have now derived a structural model of prestin and of a transport-competent ortholog by combining homology modeling, molecular dynamics and substituted cysteine accessibility scanning. The model provides a structural explanation for the anion dependence of prestin’s electromechanical activity and rationalize the relevance of previously identified protein domains required for electromotility. It provides a structural framework for deciphering the mechanistic principles of both, electromechanical activity of prestin and anion transport by SLC26/SulP transporters.