We present a hybrid microwave SQUID multiplexer that combines two frequency-division multiplexing techniques to allow multiplexing a given number of cryogenic detectors with only a fraction of frequency encoding resonators. Similar to conventional microwave SQUID multiplexing, our multiplexer relies on inductively coupling non-hysteretic, unshunted rf-SQUIDs to superconducting microwave resonators as well as applying flux ramp modulation for output signal linearization. However, instead of utilizing one resonator per SQUID, we couple multiple SQUIDs to a common readout resonator and encode the SQUID input signals in sidebands of the microwave carrier by varying the flux ramp modulation frequency for each SQUID. We prove the suitability of our approach using a prototype device and argue by means of fundamental information theory that our approach is particularly suited for reading out large cryogenic bolometer arrays.