Howey-in-the-Hills was founded by William John Howey and incorporated as "Howey" on May 8, 1925. In 1927, the name was officially changed to Howey-in-the-Hills to reflect the beautiful rolling hills and sparkling lakes, which he dubbed "the Florida Alps". Mr. Howey envisioned a great citrus empire with the Town as its commercial and shipping hub. For four years, he housed visiting prospective buyers in "Tent City", near the shore of Little Lake Harris. Long-time Howey resident, HELEN BUCK , spent her first night in Lake County in Tent City.

Town expansion accelerated in the 1950's when C. V. Griffin, Sr. promoted "Land Cruises" that lured people to the central town area where he built homes and sold them at four successful auctions. Griffin built and donated Town Hall, established Griffin Airways and was instrumental in seeing that the State Road 19 bridge linking Lake County cities and promoting commerce was constructed over Lake Harris. He was a major benefactor of the Howey Academy, founded in 1956. By the end of the 1970s, the academy had seen its days of glory, and it fell into disuse until Michael Desisto took over the operation of the facility, naming Marsha Glines, president of the new Desisto College. When the college sued the Town in federal court claiming zoning ordinances discriminated against the school's learning disabled students, the judge ruled in favor of the Town. Griffin promoted major citrus reform in Florida, was a member and committee chairman of the Florida Citrus Commission, and was a potent force in creating statewide citrus industry standards.

In 1996, residents started a series of celebrations leading up to their 75th anniversary of the Town's incorporation. In May 1997 they kicked off an annual "Birthday Bash and Citizen Salute", which is celebrated around Town Hall and the beautiful curves of Little Lake Harris, culminating in the 75th Anniversary held May 2000.