Ichinose Shima, a 16-year-old girl from the countryside, goes to attend the prestigious Aoba Art School in Tokyo. On her first day, Ichinose meets her neighbor Sarasa Ando in the girls' dormitory, but she accidentally breaks Sarasa's project for an art exhibit. As recompense, Ichinose is asked to photograph boys in the boys' dormitory; however, she is saved from that humiliating fate thanks to Akatsuki Saji. Ichinose initially thinks Akatsuki to be friendly, but she later finds his demeanor cold after conversing with him. However, to her surprise, Akatsuki chooses Ichinose to be his partner for the school festival. And so, despite not always getting along, the two begin to form a close bond through their shared passion for painting.

Crayon Days: Daikirai na Aitsu follows the cheerful Ichinose as she pursues her goal of creating extraordinary paintings, and the astute Akatsuki as he searches for the thing that his paintings lack.