At the bottom of the sea, in a deep underwater complex, a woman wakes up inside a cryogenic sarcophagus without any memories. She is greeted by the voice of Jacob, a mysterious guide that reveals bits of information about her situation, communicating through a device set on a journal. He tells that her name is Anna, and that she slept for over a century inside the chamber. She soon starts to explore outside, discovering the crumbling remains of the Ark of Humanity, created to store the greatest achievements of humankind. She must explore the surroundings, solving all the puzzles to open new avenues and uncover all the secrets of the place, as well as details about her past.
Empress of the Deep: The Darkest Secret is a traditional point-and-click adventure in the vein of Myst and other games, but with hidden object challenges and simple puzzles tailored for the casual market. The player moves between scenes by clicking on the exit hotspots, usually placed on the edges of the screen or on obvious places like doors and other openings. The context-sensitive cursor changes to an arrow when over exits, into a hand to pick objects and a magnifying glass when over a place with a zoom view showing another angle of the scene. Useful tools can be found scattered around the locations, and are automatically stored inside one of the inventory slots at the bottom after being collected, from where they can be dragged and dropped on logical portions of the scenery to perform an action or complete a task. Scenes where everything was collected and completed are marked with an "Area Complete" golden star at the top-left corner.
In some places, the scene has seek-and-find sections where the objective is to find and click on all the objects listed at the bottom, on screens filled with assorted items scattered around the area. After collecting all the items, one of the objects is stored in the inventory to be used later when solving puzzles. Mini-games appear when clicking certain places, appearing inside interactive windows where a mechanism has to be manipulated to solve a myriad of challenges, like a Tower of Hanoi variation with gears, jigsaw puzzles, a puzzle with light beams and deflecting mirrors, and other similar games.