The school was the project of Irish immigrant and Marin pioneer James Miller. The school was named "Dixie" as a dare to Miller by some builders from the American South. The school was in use for classes from 1864 until 1958. The Dixie School District gets its name from this first school.
In June 1971, the schoolhouse was moved to its current location, at 2255 Las Gallinas Avenue near Miller Creek Middle School, also in San Rafael. It was restored and renovated prior to being listed on the National Register of Historic Places in 1972.