The design of a large-scale quantum computer requires co-optimization of both the quantum bits (qubits) and their control electronics. This work presents the first systematic design of such a controller to simultaneously and accurately manipulate the states of multiple spin qubits or transmons. By employing both analytical and simulation techniques, the detailed electrical specifications of the controller have been derived for a single-qubit gate fidelity of 99.99% and validated using a qubit Hamiltonian simulator. Trade-offs between several architectures with different levels of digitization are discussed, resulting in the selection of a highly digital DDS-based solution. Initiating from the system specifications, a complete error budget for the various analog and digital circuit blocks is drafted and their detailed electrical specifications, such as signal power, linearity, spurs and noise, are derived to obtain a digital-intensive power-optimized multi-qubit controller. A power consumption estimate demonstrates the feasibility of such a system in a nanometer CMOS technology node. Finally, application examples, including qubit calibration and multi-qubit excitation, are simulated with the proposed controller to demonstrate its efficacy. The proposed methodology, and more specifically, the proposed error budget lay the foundations for the design of a scalable electronic controller enabling large-scale quantum computers with practical applications.