Age-related hearing loss (AHL) typically starts from high frequency regions of the cochlea and over time invades lower frequency regions. During this progressive hearing loss, sound-evoked activity in spiral ganglion cells is reduced. DBA mice have an early onset of AHL. In this study, we examined synaptic transmission at the endbulb of Held synapse between auditory nerve fibers and bushy cells in the anterior ventral cochlear nucleus (AVCN). Synaptic transmission in hearing-impaired high frequency areas of the AVCN was altered in old DBA mice. The spontaneous mEPSC frequency was greatly reduced (~60%), and mEPSCs were significantly slower (~115%) and smaller (~70%) in high frequency regions of old (average age 45d) DBA mice compared to tonotopically matched regions of young (average age 22d) DBA mice. Moreover, synaptic release probability was about 30% higher in high frequency regions of young DBA than that in old DBA mice. Auditory nerve-evoked EPSCs showed less rectification in old DBA mice, suggesting recruitment of GluR2 subunits into the AMPA receptor complex. No similar age-related changes in synaptic release or EPSCs were found in age matched, normal hearing young and old CBA mice. Taken together, our results suggest that auditory nerve activity plays a critical role in maintaining normal synaptic function at the endbulb of Held synapse after the onset of hearing. Auditory nerve activity regulates both presynaptic (release probability) and postsynaptic (receptor composition and kinetics) function at the endbulb synapse after the onset of hearing.