Cholinergic activity is thought to play an important role in learning and the control of brain state. Multiple studies have shown that pairing external phasic stimulation of the cholinergic basal forebrain (CBF) with a sensory stimulus drives long-lasting sensory cortical plasticity, implicating the CBF as a potential substrate for associative learning. For this to be ecologically valid, we hypothesized that CBF projections to the sensory cortex should exhibit phasic signaling that is temporally-synchronous with sensory-evoked responses in cortical neurons. Intrinsic sensory-evoked responses have previously been observed in CBF neurons but their spatiotemporal dynamics in downstream regions (i.e. sensory cortex) have not been systematically characterized. Here, we used simultaneous two-channel, two-photon imaging to examine sensory-evoked responses of CBF axon projections and cortical neurons in the ACx in mice passively listening to auditory stimuli. We observed striking, non-habituating, phasic axonal responses to neutral auditory stimuli that display an inverted-U-shaped relationship with tonic cholinergic activity – a known neural correlate of brain state. Interestingly, individual axon segments exhibited heterogeneous tuning, allowing tone frequency to be decoded from population activity. However, despite this microscopic heterogeneity, we observed no evidence of mesoscopic tonotopy in CBF axons. Furthermore, our two-color imaging approach revealed that the tuning of cortical neurons and nearby axonal segments was un-coupled, suggesting that the ACx receives de-correlated auditory signals from the feedforward auditory pathway and the CBF. Finally, we demonstrated that chemogenetic inactivation of the auditory thalamus abolished the frequency tuning of CBF axons. Our work proposes a novel, non-canonical function of the CBF in which it receives input from the auditory thalamus, modulates these signals based on brain state, and then projects the multiplexed signal to the ACx. These signals are temporally-synchronous with cortical responses but differ in their tuning, providing a potential mechanism to influence cortical sensory representations during learning.