Sharp wave ripple (SPW-R) events are brief high frequency oscillations observed throughout the hippocampal network during slow-wave sleep and quiet wakefulness. This transient synchronous activity provides the physiological scaffold for the compressed replay of awake sequences, and accumulating data support their crucial role in memory consolidation. The wide range of cortical areas that are strongly depolarized during SPW-Rs, as well as the observed coordinated reactivation of hippocampal and neocortical neural ensembles during slow wave sleep, both support the idea that memory consolidation involves the transfer of processed hippocampal information for long-term storage in distributed cortical networks. However, the majority of these cortical areas do not receive direct hippocampal projections and little is known about the routes taken by neural activity that can support this process. A prominent, yet under-investigated area that may act as a hippocampo-cortical relay is the retrosplenial cortex. Using silicon probe recordings in awake head-fixed mice, we report here the coordinated interplay of retrosplenial and hippocampal activity during SPW-Rs and the existence of SPW-Rs analogues in the retrosplenial cortex. We show that these interactions are topographically organized and layer specific. Using large-coverage high-density recordings, we demonstrate the existence of multiple subclasses of SPW-Rs and show that retrosplenial neurons are tuned to specific constellations of hippocampal output during SPW-Rs. Finally, we show that hippocampal output to the retrosplenial cortex is mediated by a genetically defined subpopulation of subicular bursty neurons. We demonstrate that optogenetically stimulating these vesicular glutamate transporter 2-expressing neurons is sufficient to evoke cortical ripple responses in superficial retrosplenial cortex, while optogenetic inhibition significantly reduces such responses. These results yield a mechanistic understanding of the neural substrate underlying hippocampal-cortical interactions during the awake resting state, and provide insights into how the offline transfer of previously stored information from the hippocampus to the cortex may be coordinated.