The cranes were among two dozen such heavyweight hazards looming over the city skyline as the monster storm powered across the state.
No injuries were reported after either crash, said Miami City Manager Daniel Alfonso.
The first crane fell in a bay-front area filled with hotels and high-rise condo and office buildings, near the AmericanAirlines Arena, where the NBA's Miami Heat play.
VIDEO: SECOND CRANE COLLAPSE IN MIAMI
It was stationary after the collapse, according to the contractor operating the crane.
"All possible preparations and precautions were taken, but we believe that a micro-tornado struck this area, compromising the crane. Again, we're grateful there have been no injuries," said John Leete, Moriarty executive vice president.
A crew will be dispatched to secure the crane as soon as weather conditions improve, developer Ryan Shear, a principal of Property Markets Group, said in an emailed statement.
"All we care about is the safety of everyone right now," Shear said.
The second crane collapsed at another site farther north along the water. The site has multiple towers in the Gran Paraiso by the Bay development, Alfonso said.
The city has contacted the Occupational Safety and Health Administration and neighbors in nearby buildings, Alfonso said.
Some two dozen other cranes in the city remained upright. There wasn't time before Irma approached Florida to move the massive equipment, with counterbalances weighing up to 30,000 pounds.
VIDEO: STORM SURGE FLOODS MIAMI
Moving the cranes would have taken two weeks, city officials said. Only a few companies are certified to do that kind of work, said Dan Whiteman, vice chairman of Coastal Construction, who has 12 cranes in the Miami area.
Abby Ape's 14th-floor apartment has a view of the toppled crane.
"We heard a loud crack toward the bay," Ape said. "The top portion that most people see is broken in half."
She also could see another nearby crane spinning, and she said her family was prepared to run into a stairwell for safety.
"In the future there should be an easy way to bring them down in events like this one," Ape said.
Though 110 miles (180 kilometers) from Irma's landfall in the Florida Keys, hurricane-force winds from the 400-mile-wide storm were being felt through the Miami area. Gusts over 90 mph (145 kph) were reported at Miami International Airport.
The National Hurricane Center said winds hitting upper floors of high-rise buildings are significantly stronger than near ground level.
The city and surrounding areas were under a tornado watch Sunday.
Officials urged people in buildings facing the crane to seek shelter on the opposite side of the building or in a stairwell.
Whiteman said videos of the first collapse posted on social media showed a tower crane that appeared to have lost its jib or boom, though its mast was still standing.
The same videos showed his tower cranes spinning in the background.
"Our cranes are still weather vane-ing," Whiteman said. "But for the grace of God, that (collapse) could be me."
Only a few contractors are certified to remove those cranes, he said.
Tower cranes can rise hundreds of feet into the air on steel frameworks, and are used to lift steel, concrete, heavy construction equipment and other building materials.
The horizontal arms of some cranes were left loose to spin in the winds. The equipment was designed to withstand winds up to 145 mph (233 kph), city officials said.
A tornado could have ripped the crane loose, Whiteman said.
"Hurricane winds are blowing in one direction but a tornado could twist things, and nothing can be designed to withstand the tornado effect," Whiteman said.
Miami Heat officials said some of the arena's exterior paneling was damaged, but there was no structural damage.