Neither of Buttermilk's parents wanted him. He was born out of duty, nothing more. His parents shared no love for each other, and gave none to him. After the Overseer's daughter was born, Buttermilk had been promised to her as her future husband. He and Winterwillow were raised close together, knowing that they'd one day have to run the stable together. While Winter had always been madly in love with him, Buttermilk only ever viewed her as his little sister. She was his only solace in life, his very best friend, but he felt no romantic love for her. He felt no romantic love for any mare. He much preferred the company of stallions.

Buttermilk was very young, having just earned his cutie mark, when his father was charged with murder and executed. His mother, Mascarpone, told him it was because of the deer, that everything bad in their lives was always the fault of the deer. He didn't understand, but his mother's constant lessons and pressure drove a wedge between him and any deer that he met. The only deer he associated with in the entire stable was Winter, who was half pony. His future wife fought every day of her life to unite the deer and pony populations, and Buttermilk supported her, but he always secretly felt that her efforts were futile. Harmony with the deer was an impossible dream.

It wasn't until Winterwillow succeeded her father and became the official Overseer of the stable that Buttermilk learned his father had never been executed at all, but was imprisoned in a lower level of the stable that not even the deer visited. Overseer Whitecliff could not bear to kill his best friend, even though he had murdered his wife. Buttermilk visited his father only one time. He was met with vile anger that had only built up and grown stronger over the years Oleander had been locked away. Perhaps he would have visited again and attempted to battle his father's anger, had the stable not been attacked.

Whitecliff had taught Buttermilk safety protocols that were kept secret even from Winter. In the event of catastrophe, the Overseer had to be kept safe. He and Winter were sitting in her office, only a week after her ceremony, when the alarms went off. Buttermilk sprang into action, revealing a secret passage, and escorted her to safety. They followed the passage all the way out of the stable into the cellar of a pre-war home. Following Whitecliff's directions, the two hid in this cellar for four entire days, relying on the rations stocked inside in case of emergency.

After four days, Buttermilk and Winterwillow followed the passageway back down into the stable to find their home empty. Doors had been knocked down, rooms had been ransacked, and any usable food or material was gone. There were bodies, but nearly not enough. The majority of the stable residents had been taken somewhere, stolen right out of their home. Winterwillow, being the loving leader that she is, tasked herself with tracking down her ponies and deer and finding out what happened to her stable. Buttermilk followed, fully believing that if anyone had the strength to face the outside world and survive, it was her.