The summating potential (SP), the DC potential which, along with the AC response, is produced when the hair cells convert the vibrational mechanical energy of sound into electrical signals, is the most enigmatic of the cochlear potentials because its polarity and function have remained elusive for more than seven decades. Despite the tremendous socioeconomic consequences of noise-induced hearing loss and the profound physiological importance of understanding how loud noise exposure impairs the hair cell receptor activation, the relationship between the SP and noise-induced hearing impairment remains poorly characterized. Here, I show that in normally hearing ears, the SP polarity is positive and its amplitude relative to the AC response grows exponentially across frequencies, and becomes negative and decreases exponentially across frequencies following noise-induced hearing injury. Since the SP is thought to be generated by K+outflow down the gradient through the hair cell basolateral K+channels, the SP polarity switch to negative values is consistent with a noise-induced shift in the operating point of the hair cells.Supplementary InformationThe online version contains supplementary material available at 10.1007/s00018-023-04809-5.