Ys VI: The Ark of Napishtim is a direct sequel to Ushinawareta Suna no Miyako Kefin, the fifth installment of the Japanese action RPG series. Once again, the player controls the main character of the series, the adventurer Adol Christin, on a new journey. Adol's ship has been attacked, and he loses his consciousness. After a while, he wakes up on a sea shore, rescued by the Rehda, elf-like people who live in a small village. Soon he becomes involved in a quest for mysterious treasure hidden somewhere on nearby islands, and has to face an ambitious empire officer who will not tolerate any rivals on his hunt.

The Ark of Napishtim is an action role-playing game set (for the first time in the series) in a fully 3D environment. The game world is seamless, with transitional overworld areas connecting dungeons and settlements. Much of the game takes place in hostile areas, where the protagonist engages in fast-paced action combat against regular enemies and bosses. Like its immediate predecessor, the game abandons the "bumping" combat style of the earlier installments, opting instead for the more common active combat. Adol can execute regular attacks and jump, as well as combine those for upward and downward slashes, dash attacks, and longer jumps. Experience points and money are awarded for defeating enemies, and leveling up is fully automatized. Armor and accessories can be found in treasure chests or purchased.

There are only three swords during the game, each corresponding to a particular element. Each sword comes with its own unique magic spell. These swords can be leveled up in a specific workshop by spending blue crystals known as "emel", which are dropped by enemies. As the swords level up their attack power increases, and their respective magic spells gain levels and become more damaging as well.