Ultimately the goal is to open the mysterious 5th dungeon, but in order to do that the player must first unlock each of the first four dungeons and defeat the guardian inside. Progress is made in the game in a few different ways. This opens up the opportunity to craft weapons, armor, and potions, as well as to purchase decorative items for your shop and other things. As the game progresses, the player can invest in the town and invite other merchants to come and set up shop. The town of Rynoka is initially home to just one store, Moonlighter, owned by the player. This pendant will cost some gold to activate, so make sure you have some gold stored up before going to a dungeon, otherwise you'll be forced to use the Merchant's Mirror (more below) or pass out. When a player has collected a full load of treasure (or simply is too injured to go on), they can activate a magic pendant that generates a warp back to town. Each of the five dungeons has a different theme and the player will find related items when they defeat enemies in that dungeon.

The player enters procedurally generated dungeons and explores them in search of treasures to sell in their shop. As the game title suggests, the player is essentially 'moonlighting' as an adventurer at night and working as a shop owner by day. Moonlighter combines the action and adventure elements of a roguelike dungeon crawler with the magic of a shop management simulator.

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