The film's story is set four years after the events of the original Shirobako anime. Aoi Miyamori keeps busy dealing with the ordinary troubles in her daily work at Musashino Animation. After a morning meeting, Watanabe talks to Aoi and puts her in charge of a new theatrical anime project for the studio. The project has unexpected problems, and Aoi is unsure if the company can proceed with a theatrical anime with its current state of affairs. While dealing with that anxiety, Aoi meets a new colleague named Kaede Miyai (voiced by Ayane Sakura). She and the MusAni team work together to complete the project.

Thirteen years after achieving major success with the Indiana Hornets, Gorou Honda's career as a pitcher ended abruptly after sustaining a horrible injury. Inspired by his father, who continued playing baseball despite major setbacks, Gorou plans to restart his baseball career and play in a new position. However, his strong dedication to train has puzzled his family, especially his young daughter Izumi, who is frustrated with the absence of her father from her lives. Faced by another tough obstacle, Gorou once again decides to prove his resolve through his beloved sport. [Written by MAL Rewrite]

Taka (technically Tamahome) and Miaka are now happily married and only six months before their new family would be born, but an obsessed girl named Mayo would do anything to make Taka hers. She enters the world of the Four Gods, determined to win Taka's heart and be the new priestess.

Continuing where the first season left off, the sudden increase of Thanatos with the disappearance of the Aube Hunters has now left Arcadia in ruin. Desperation reigns high as the Religious Organization fights to battle the Thanatos. Six months had already past since Hidamari mansion burned to ashes, the Aube Hunters, once hailed as heroes, is now blamed for the appearance of Thanatos. Nevertheless, hope still exists for the reappearance of the Queen's Egg one day, who will become the savior of Arcadia. Unknown to many however, the Aube Hunters have actually been silently waiting for the awakening of Angelique, who has been asleep the entire time.