The hippocampus is crucial for episodic memories and is characterized by unique sharp wave ripple complexes (SWRs). These hallmark oscillations, 150-250 Hz in the local field potential (LFP), are produced by fast signaling between synaptically coupled pyramidal neurons (PNs) and parvalbumin-positive basket cells (PV+BCs). Although much has been learned about the synaptic and microcircuit properties mediating ripple oscillations, whether and how myelination of the hippocampus contributes remains unresolved. Here, we performed LFP measurements in combination with paired recordings between PV+BCs and CA1 PNs in acute hippocampal slices from PV-Cre ´ Ai14 mice and made use of a toxin demyelination model (cuprizone) in which oligodendrocytes and myelin are transiently disrupted. While PN axons were only myelinated in the alveus, around extrinsically projecting long-range axons, the PV+BC axons were densely myelinated in stratum pyramidale (SP) and stratum oriens (SO) where they form local connections that are functionally relevant for the SWR. Cuprizone-mediated demyelination selectively affected oligodendrocytes in SP and SO subfields, causing a near-complete loss of myelin and nodal domains of PV+BC axons. In accordance, cuprizone demyelination delayed unitary inhibitory synaptic transmission (~300 ms) but not the unitary excitatory connections and in parallel increased the excitability of deep CA1 PNs. Furthermore, demyelination was associated with a slowing of the internal SWR frequency by ~20 Hz. These data indicate that PV+BC myelination critically tunes SWRs with sub-millisecond precision. Oligodendroglial myelination may thereby compress PN reactivation during neuronal replay to facilitate memory consolidation, providing a mechanistic basis of cognitive deficits in demyelinating diseases.