Avondale Estates was founded in 1924 by George Francis Willis, a patent medicine magnate, who purchased the entire village of Ingleside to create a planned community. The city was named after Stratford-upon-Avon, England, birthplace of Shakespeare. Downtown buildings were designed in a Tudor style to reinforce this image, as were many of the houses in the city. The city incorporated in 1927.
The mostly Tudor-style downtown area of Avondale Estates, known as the commercial district, is home to a variety of businesses including consignment stores. Pizza, southern comfort food, and Chicago style hot dogs are some of the restaurant fare options within the city limits. The city is the location of the first Waffle House restaurant which opened on Labor Day weekend in 1955 having been converted into a museum, along with an existing operational full-time Waffle House nearby, with numerous others in the Decatur, Georgia area as well. The Avondale Salad, featured on certain Waffle House lunch menus, derives its name from the city. A selection of art galleries and studios are in an area of the city known as the Rail Arts District. Little Tree Art Studios located on Franklin Street, is a warehouse that includes multiple artist studios and a music rehearsal space.
The movie, Instant Family (2018), starring Mark Wahlberg, was filmed in Avondale Estates.
Avondale Elementary School is in the city limits. Druid Hills Middle School, and Druid Hills High School serve the community.