The 26,000 square foot building replaces an old windowless structure built in the early 1980s, The St. Petersburg (Fla.) Times reported.
Commander Gen. James Mattis thanked Congress for approving the project and taxpayers for financing it at Monday's dedication.
The total cost of the project is expected to hit $82 million, which includes the demolition of the old building.
The new facility has an entire floor dedicated to a global communications network.
The windows will improve morale, said Army Maj. Gen. Karl Horst, CentCom's chief of staff.
And because the layout is more logical, it's easier to find people, Horst said.
Some 2,000 people work at CentCom headquarters.