Embodiments disclosed herein are related to systems and methods for implementing a customizable compact overlay window in a display. In one embodiment, a computing system includes one or more processors and a storage device that stores computer executable instructions that can be executed by the processors to cause the computing system to perform the following. The system receives from an application running on the computing system customization parameters that define how the application is to be configured in a compact overlay window. The system generates the compact overlay window so that the compact overlay window is customizable according to the customization parameters. The system positions the compact overlay window in a portion of a display of the computing system.