Asura's Wrath is an action game where the player controls the titular Asura. He is one of the eight elite demigods, and their main Guardian General, who leads a legion to fight a race of beasts called Gohma who roam Earth, called Gaea in the game. He serves the emperors who rose as the leaders of Shinkoku Trastrium, a civilization that unified all nations. Demigods derive their power from mantra, a source powered by the emotion of mortals. The civilization however drained the planet of its resources and the Gohma was a natural phenomenon to combat the power of Shinkoku Trastrium. It leads to the War of Creation which neither side can win. Eventually Vlitra is awakened, a Gohma the size of the continent that causes the demigods to erect Karma Fortress, an orbital space station. The game starts when the Gohma attack the space station and specifically a giant laser known as Brahmastra, powered by mantra, that could wipe out all Gohma. Asura's daughter Mithra is chosen by the 128th Emperor Strada to become the main priestess to guide the mortal's prayers to provide mantra, but the appointment is not to Asura's liking. The main story is split up into three parts with 18 episodes in total. These follow the style of an anime series with opening and ending credits, including cut-scenes and a preview of the next part of the story at the end. Next to a hidden ending the game's story is further extended through DLC with a fourth part, lost episodes, and extensions of existing episodes.

Large parts of the game are played as a third-person fighting game with a focus on melee combat. Asura has different attacks that can be chained into combos. Heavy attacks cause him to overheat however and cannot be used continuously. There are dive attacks to engage from the air, dash to break through shields and a quick recovery attack to reduce damage after being hit, along with regular counters and dodging. He also has a ranged cannon that can lock onto enemies and blast opponents and projectiles out of the sky. By inflicting and receiving damage an Unlimited gauge near the top of the screen is filled up. Once full it can be activated for the Unlimited mode for more strength and no overheating. Next to the green health bar there is a red Burst gauge filled up by defeating enemies, inflicting damage, and following on-screen prompts. Once full a powerful attack is unleashed and that one is often needed to finish off the most powerful opponents and advance the plot.

For many parts the game shifts into rail shooter sequences where Asura soars through the skies. In those sequences movement is limited to a fixed axis for the area shown on the screen and the camera rotates automatically. Asura attacks and locks onto multiple targets and needs to evade projectiles Space Harrier style. The game has many cinematic events that require direct input from the player. These appear during gameplay but also during static cinematics or flight sequences. These quick-time events are rated based on accuracy and speed, and even during cinematics missing them can cause Asura to die or lose a significant amount of health.