Minutes after liftoff and booster separation, a live video feed showed the upper stage tumbling uncontrollably before the signal abruptly cut.
Dramatic footage circulating online showed red-hot debris raining down over the Bahamas.
"Can confirm we did lose contact with the ship. Unfortunately, this happened last time, too," SpaceX spokesman Dan Huot said, referring to January's flight, which also ended with the upper stage disintegrating over the Caribbean.
The fallout immediately impacted US airspace.
The Federal Aviation Administration (FAA) briefly activated a "debris response area," delaying flights from airports stretching from Newark and Philadelphia to Miami.
The agency confirmed SpaceX will be required to conduct an investigation before it can fly again.
SpaceX said in a statement that an "energetic event in the aft portion of Starship" had "resulted in the loss of several Raptor engines."
"This in turn led to... ultimately a loss of communications with Starship," it said, adding there were "no toxic materials present in the debris."
"We will conduct a thorough investigation, in coordination with the FAA, and implement corrective actions."
Despite the setback, SpaceX's "fail fast, learn fast" approach has helped it become the world's dominant launch services provider.
But Musk's status as one of President Donald Trump's closest advisors, and his influence over federal regulators, are raising concerns about potential conflicts of interest.
- Eighth Starship Test -
Starship -- the world's largest and most powerful rocket -- lifted off from SpaceX's Starbase facility in Boca Chica, Texas, shortly after 5:30 pm (2330 GMT).
It marked its eighth uncrewed orbital test, after launch attempts were scrubbed on Monday and Wednesday.
While the upper stage was lost for a second consecutive flight, SpaceX successfully recovered the Super Heavy booster, catching it with the launch tower's mechanical "chopstick" arms for the third time -- an impressive feat of engineering.
About 40 minutes after launch, SpaceX ended its livestream, without providing further details.
Standing 403 feet (123 meters) tall -- about 100 feet taller than the Statue of Liberty -- Starship is designed to eventually be fully reusable and is key to Musk's long-term vision of colonizing Mars.
NASA is also awaiting a modified version of Starship as a lunar lander for its Artemis program, which aims to return astronauts to the Moon this decade.
But before SpaceX can carry out those missions, it must prove the vehicle is reliable, safe for crew, and capable of complex in-orbit refueling -- critical for deep space missions.
The FAA previously grounded Starship after its January 16 flight ended in an upper-stage explosion.
Last Friday, the agency allowed SpaceX to proceed with this latest test before finalizing its investigation into that explosion.
- Conflicts -
During Joe Biden's presidency, Musk frequently clashed with the FAA, accusing it of over-regulating SpaceX over safety and environmental concerns.
Now, as Trump's chief advisor on cost-cutting initiatives, Musk faces scrutiny over his influence on federal agencies overseeing his companies.
According to Bloomberg News, a SpaceX engineer recently visited FAA headquarters, warning employees their jobs were at risk if they did not begin work on a program to deploy thousands of the company's Starlink satellite terminals in support of the national airspace system.
Telecom giant Verizon holds a contract to upgrade the FAA's infrastructure, but that deal could be in jeopardy, Bloomberg reported.
SpaceX has denied the allegations, stating "recent media reports about SpaceX and the FAA are false."
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