Genie-girl Shantae is the self-appointed guardian of a small fishing village, Scuttle Town. Living life in a lighthouse rather than a bottle, she's constantly on the lookout for danger. When the nefarious lady-pirate, Risky Boots catches wind of the treasure that was recently unearthed in the village, she launches an attack. To get Scuttle out of trouble, it's up to Shantae to prove that she's the rightful 'Guardian Genie' to the best of her dancing, buying and hair-whipping abilities. Now crack that whip!

A gang of pirates, the Tinkerbats, led by Risky Boots, attacks Scuttle Town and steals a prototype steam engine from Mimic, the town's resident treasure hunter. Mimic tells Shantae, the guardian of Scuttle Town, that if Risky retrieves four magical "elemental stones", she could power up the steam engine and create an unstoppable weapon out of it. Shantae travels across Sequin Land, determined to retrieve the steam engine and the elemental stones and stop Risky.

With help from her friends Bolo and Sky and her acquaintance Rottytops, she gains access to three dungeons where she retrieves three of the stones. At the fourth dungeon, Shantae finds the fourth stone, but is ambushed at the exit by Risky, who leaves with the stones. Shantae subsequently discovers the location of Risky's hideout with a magical flying telescope called the Sky Scope, and teleports there. Shantae reaches and destroys Risky's weapon, the Tinker Tank. Risky tries to kill Shantae but is defeated; and as Risky's hideout collapses, Shantae escapes. After, she is magically abducted to a place called the Genie Realm where the genies offer her a chance to remain with them as a reward for her courage, but at the price of never seeing her friends again. She refuses and is sent back to Scuttle Town where she announces to Mimic that she had to destroy the steam engine, but is relieved to hear from him that it was probably for the better.