Ōkamiden was designed by Kuniomi Matsushita, the director of the Wii port of Ōkami, and Motohide Eshiro, producer of Ace Attorney Investigations: Miles Edgeworth and Onimusha 2: Samurai's Destiny.

Because the demo was so well-done, development began on a sequel, and in September 2010, four years after Ōkami debuted, the game was released to positive reviews from critics and moderate commercial success.

The game uses the face buttons to move Chibiterasu about the world, with the top display being the current third-person view and the bottom showing a mini-map of the area.

Producer Eshiro noted that he is a "young form of existence" and not fully grown; he retains several abilities of Amaterasu, including the Celestial Brush, but lacks her power, which will be reflected in the plot and gameplay.

[9] Other partners include: Nanami (ナナミ), a young mermaid that is able to swim about in underwater stages and can provide a water source for Waterspout; Kagu (カグラ, Kagura), a spirit medium who helps Chibiterasu see ethereal elements; Kurow (クロウ, Kurō), a flute-playing young boy that bears some traits similar to Waka from Ōkami; and Manpuku (マンプク), an overweight boy carrying fire who can walk through ice spikes and can provide a fire source for the Inferno technique.

[16][18][19] Chibiterasu and his various partners initially track down an evil summoner named King Fury (怨霊王, Onryō-ō) that gave rise to the curses across the lands.

Furious, Akuro travels back 100 years in time, when the swordsman Nagi and Shiranui, the wolf form that Amaterasu was later given, defeated Orochi.

Chibiterasu and his other allies follow Akuro to the dark realms where they find the demon has taken up residence in the body of Kuni and that Kurow intends on fighting the pup.

Chibiterasu is forced to fight his former partner, expelling Akuro's spirit and freeing Kuni, but evil Kurow willfully allows it to take his body.

Ōkamiden was directed by Kuniomi Matsushita, who oversaw for the Wii port of Ōkami, and was produced by Motohide Eshiro, who had previously worked on titles such as Onimusha 2: Samurai's Destiny and Ace Attorney Investigations: Miles Edgeworth.

The team settled on the Nintendo DS due to its portability, allowing players to pick it up and play wherever they wish, as well as the utility of the stylus on the touch screen acting as a brush.

The work Clover did was amazing; they were really talented people, and I think our staff now is motivated to make a game that lives up to the reputation of the previous Okami.Eshiro further commented that he considered Ōkamiden more of a successor to Ōkami than a sequel, desiring to build upon the world for a franchise on the Nintendo DS platform.

[28] One change made from Ōkami was the simplification of the combat system, a factor that some players had found difficult; Ōkamiden reduces the melee weapon attack features down to a single button, but the Celestial Brush can still be used alongside this for complex strategy.

[15] While there were significantly more Celestial Brush strokes and puzzles the team wished to add, they left these out in the final version, feeling they had added too much padding to the game.

[15] The number of polygons and the resolution of the artwork was prohibitively limited on the DS version, challenging the artists to convey similar imagery and emotions that were in the first game.

[32] Using a story taken from a child's point of view as they explore and learn new things made the game much easier to visualize (and incidentally fell in line with the core demographic of Nintendo handheld devices).

[32] Eshiro also felt it was important to include making friends and having to say goodbye as part of this adventure, striking a strong emotional aspect to the game.

[32] The game takes place nine months after the events of Ōkami, which posed story problems for Yukinori Kitajima, Ōkamiden's main scriptwriter.

[36] A series of television advertisements in Japan for Ōkamiden feature model Kii Kitano and a white Shiba Inu puppy named Moran-chan that bears a close resemblance to Chibiterasu.

[37][38] North American pre-order bonuses included an Ōkamiden-stylized screen cleaner and brush-shaped stylus at GameStop[39] and a plush Chibiterasu key chain (identical to the Japanese collector's edition) at the Capcom Store.

The Escapist editor John Funk stated that it was the perfect platform for the sequel, due to how the touch screen could be used effectively for the Celestial Brush.

[43] Siliconera editor Ishaan Sahdev, however, was skeptical that Ōkamiden could replicate the feel that Ōkami provided, due to how much it relied on its visuals and art style to bring players into its world.

[48] Destructoid editor Jim Sterling concurred, joking that its cuteness would make Ōkamiden one of the greatest Nintendo DS games ever made.

[69] GameZone gave the game a 7/10, stating: "There are some players who will undoubtedly love Ōkamiden, either because the flaws (such as backtracking) are not as familiar or because they have the capacity to overlook its myriad mistakes.