Deformable mirrors (DMs) are a critical technology to enable coronagraphic direct imaging of exoplanets with current and planned ground- and space-based telescopes as well as future mission concepts, such as the Habitable Exoplanet Observatory and the Large UV/Optical/IR Surveyor. The latter concepts aim to image exoplanet types ranging from gas giants to Earth analogs. This places several requirements on the DMs such as requires a large actuator count (≳3000), fine surface height resolution (≲10  pm), and radiation hardened driving electronics with low mass and volume. We present the design and testing of a flight-capable, miniaturized DM controller. Having achieved contrasts on the order of 5  ×  ^{10  −  9} on a coronagraph testbed in vacuum in the high contrast imaging testbed facility at NASA’s Jet Propulsion Laboratory (JPL), we demonstrate that the electronics are capable of meeting the requirements of future coronagraph-equipped space telescopes. We also report on functionality testing on-board the high-altitude balloon experiment “Planetary Imaging Concept Testbed Using a Recoverable Experiment – Coronagraph,” which aims to directly image debris disks and exozodiacal dust around nearby stars. The controller is designed for the Boston Micromachines Corporation Kilo-DM and is readily scalable to larger DM formats. The three main components of the system (the DM, driving electronics, and mechanical and heat management) are designed to be compact and have low-power consumption to enable its use not only on exoplanet missions, but also in a wide-range of applications that require precision optical systems, such as direct line-of-sight laser communications. The controller is capable of handling 1024 actuators with 220 V maximum dynamic range, 16-bit resolution, 14-bit accuracy, and 1 kHz operating frequency. The system fits in a 10  ×  10  ×  5  cm³ volume, weighs <0.5  kg, and consumes <8  W. We have developed a turnkey solution reducing the risk for future missions, lowering their cost by significantly reducing volume, weight, and power consumption of the wavefront control hardware.