The Destin Library was founded in 1940 as a volunteer-run community lending library. Housed in the Sunday school room of the First Presbyterian Church on Calhoun Avenue, the library consisted of approximately 200 volumes. The collection was largely the result of one man's generosity: Mr. Albert Fox of Syracuse, NY donated the books for the express purpose of founding a library in the village he would eventually call home. The library collection was housed in several different facilities over the years; after outgrowing the church it was moved to the upper floor of the old Destin Community Center building, and then to the purpose-built library across the street at 108 Stahlman Avenue. The Stahlman Avenue library was expanded to include a thrift shop to support library operations by the Friends of the Destin Library. (That building now houses the Destin History and Fishing Museum.)
In 1989, five years after the City of Destin was incorporated as a self-governing municipality, the Destin Library was added as a department of the City government organization. The Friends of the Destin Library continue to support library programming and facility improvements. In 2002 ground was broken for the new Sibert Avenue library facility, and its doors officially opened to the public on St. Patrick's Day of 2003. This 13,000 square foot facility continues to evolve, with the addition of private study rooms and a digital media lab in 2014.