An information handling system plays audio provided from a portable audio device at an information handling system audio subsystem in operating and powered down states of the information handling system. In the operating state, digital audio information is communicated from the portable audio device through a serial link for rendering at the information handling system into an analog audio signal presented by the audio subsystem. In the powered down state, digital audio information is rendered at the portable audio device and communicated as an analog audio signal through the serial link to the information handling system. A system module at the information handling system selectively switches the serial link to interface with the audio subsystem and play the analog signal as audible sounds. The system module supplies power to the audio subsystem to support playing the analog signal with the information handling system in the powered down state.