We propose an efficient microwave-photonic modulator as a resource for stationary entangled microwave-optical fields and develop the theory for deterministic entanglement generation and quantum state transfer in multi-resonant electro-optic systems. The device is based on a single crystal whispering gallery mode resonator integrated into a 3D-microwave cavity. The specific design relies on a new combination of thin-film technology and conventional machining that is optimized for the lowest dissipation rates in the microwave, optical, and mechanical domains. We extract important device properties from finite-element simulations and predict continuous variable entanglement generation rates on the order of a Mebit/s for optical pump powers of only a few tens of microwatts. We compare the quantum state transfer fidelities of coherent, squeezed, and non-Gaussian cat states for both teleportation and direct conversion protocols under realistic conditions. Combining the unique capabilities of circuit quantum electrodynamics with the resilience of fiber optic communication could facilitate long-distance solid-state qubit networks, new methods for quantum signal synthesis, quantum key distribution, and quantum enhanced detection, as well as more power-efficient classical sensing and modulation.