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Ave Maria was founded in 2005 by Ave Maria Development, a partnership consisting of Barron Collier Companies and the Ave Maria Foundation led by Catholic entrepreneur Tom Monaghan, founder of Domino's Pizza and Ave Maria University. The development of the town was made possible when the Florida legislature created the Ave Maria Stewardship Community District, a limited local government whose purpose is to provide community infrastructure. The town was the first to develop under the Rural Lands Stewardship Area (RLSA) program.2025 marked the 20th anniversary of Ave Maria’s groundbreaking. Since its establishment in 2005, the community of Ave Maria has sold over 5,000 homes, resulting in the emergence of new businesses, including the Midtown Plaza, which will house various retail establishments to support local economic growth.

Monaghan's goal was for the town to be especially attractive for Catholics to move to. Many of the street names are Catholic in nature, and the center of town is anchored by a large Catholic church. During a 2007 interview,Monaghan insisted "[Ave Maria town] is open to everyone, not just Catholics". Fellowship Church is a Baptist church in Ave Maria that was founded in 2017.

In a 2007 interview with CNN, Monaghan stated that his 10-year plan was for Ave Maria to have 11,000 homes, 25,000 residents and 5,000 students at Ave Maria University. He wanted to build a community where "a particular number of Catholics, particularly serious Catholics, would want to live around a really high-quality Catholic university."

Ave Maria was ranked 18th in the US for planned community home sales in 2024.

In June 2023, Collier County commissioners approved the expansion of Ave Maria by 1,000 acres. This brought the town's size to 5,000 acres, which is the largest allowed under the county rules.The Ave Maria University campus is not included in this acreageThe new land will be used mainly for single family homes, as well as a new town center and additional retail sites.

Ave Maria experienced a surge in new businesses in 2024, particularly within the Midtown Plaza development, adding diverse dining and retail options for residents. This commercial growth was implemented due to strong residential sales and planned expansion, including new healthcare and restaurant offerings. Future development is anticipated with available out-parcels and a rezoned area near the town's entrance, promising continued commercial growth alongside the increasing population.

It was announced in October 2024 that the master-planned community in Collier County is expanding commercially with Midtown Plaza. They will be adding businesses like LEDO Pizza, Sunshine Ace Hardware, Dunkin', Cold Stone Creamery, and more, with an immediate care center and restaurant planned for 2025.This growth reflects the increasing population of Ave Maria and Collier County, providing convenient amenities and reinforcing the community's family-oriented focus.