A few years have passed since Luna returned to Equestria's peaceful embrace and she intends to keep it that way without her subjects' knowledge. Feeling she owes Equestria a debt she cannot repay, she personally carries out covert operations against would-be aggressors of her nation. Celestia forces her to take a partner, and the seeds of a reluctant friendship are sowed.

When Celestia sends Amber, a protector of the border between the Changeling Grounds and Equestria, Twilight is excited to help her learn about friendship. However, Amber proves to have more baggage than Twilight had expected. With trouble finding her at every turn, Amber shows that she is claustrophobic, insecure, and attracts a fair share of enemies, both real and hallucinated.

After Equestria mobilizes to help a neighbouring empire after an earthquake strikes its southern region, Twilight and company find out that an ancient demon has returned from it's imprisonment. Now, they must team up with a mysterious lone colt and set out to stop this demon from destroying the world.

In the future, the three separated races of ponies engage in a world war as resources become scarce and relations between races become hostile.