The story takes place in Manehatten where a mutated version of Cutie Pox known as Bit Poison has devastated the government of Equestria. The Strategic Homeland Division is activated to save what remains and preserve the government. They are sent to Manehatten to help liberate the city from three hostile factions. The Ravagers, The Followers, and the Wolf Private Army.

The main character is Shadow Dawn. A bat pony activated in the second wave. But she will work together with three other agents. Autumn Rush, Cloud Dancer, and Rain Rider. While trying to liberate the city. Shadow Dawn will also try to piece together what happened to the first wave of Division agents.

When Princess Celestia was imprisoned upon Nightmare Moon's return, Equestria was left leaderless and afraid in the dark, resulting in widespread panic and looting across the nation. Although Celestia was quickly able to restore peace after her return, the situation troubled her greatly. In order to prevent something like this from happening again, she signed Directive 51 into law, establishing the Shadowbolt Harmony Division, an elite group of soldiers that operate independently in the most hostile of circumstances in order to eliminate threats and maintain order.

Years later, a mysterious illness of unknown origin ravaged the city of Manehattan, and the EUP guard were unable to control the mass of rioters. The city fell into chaos, and when the Princesses arrived to restore order, they became infected themselves. The Division was activated in response, sending in agents to reinforce the EUP soldiers in retaking the fallen city.

Originally designated as a second-wave reinforcement, Agent Rainy arrives in Manehattan to find that the first wave has disappeared, with rioters roaming free in the streets. Alone and against the odds, she must find a way to retake the city and find a cure... but rioters aren't the only enemies out to stop her.