The Tampa Bay History Center contains 60,000 square feet of exhibits depicting almost 500 years of human history in the Tampa region. Visitors can walk through a 1920s-era cigar store, boat up the Hillsborough River, ride along with a cattle drive, and learn about the early exploration of Florida in a dramatic theater presentation. Other exhibits include Coacoochee's Story Theater, which offers a riveting account of Seminole Chief Coacoochee's experiences during the Second Seminole War; Florida's First People, which features Tocobaga and Calusa artifacts, including tools, weapons, and pottery, as well as original artwork by artist Theodore Morris; and Cigar City, which showcases Tampa's cigar industry and immigrant communities while featuring one of the most extensive cigar memorabilia collections in the world. The waterfront History Center boasts a remarkable atrium, interactive and immersive exhibits, theaters, a map gallery, a research center, an event hall, an eclectic museum store, and the Columbia Cafe. The 2,800-square-foot Third Floor Gallery houses a rotating schedule of exhibitions.

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