The United States, which has thousands of troops stationed on the southern island, had previously ignored requests to ground the aircraft after a CH-53D swiped a campus building before crashing into university grounds in a built-up area on August 13.
Three crew were hurt in the crash.
"US Forces Japan will not fly Marine Corps CH-53D helicopters until it is appropriate to do so," the US embassy in Tokyo said in a statement.
"The government of the United States deeply regrets the crash that occurred in Ginowan city."
Six CH-53Ds took off from Okinawa last Sunday despite Tokyo's insistence the craft be grounded until preventive measures were taken and an official explanation given.
Ginowan Mayor Yoichi Iha protested to the US over the resumption of flights.
Around 44,600 US troops are based in Japan, two-thirds of whom are stationed in Okinawa where tensions run high over their presence.