The US spends more than $9m (£5.7m) a day on the war against Islamic State, and has poured $2.7bn (£1.7bn) into the bombing campaign since the start.
An international coalition has been conducting air strikes in Iraq and Syria since last August.
The first breakdown of US costs, released by the Pentagon, show that two-thirds of the total bill has gone to the Air Force.
It came as Congress rejected legislation banning further spending.
The US House of Representative approved a $579bn defence spending bill.
It rejected an amendment calling for a stop to cash going on the fight against IS unless Congress passed a new authorization for the use of force.
The cost of the US military operation has risen sharply since it began last August in Iraq.
This week, the White House announced another 450 advisers for Iraq, bringing the total military personnel to 3,500.
But officials emphasise there are no combat troops and the US mission is to train local forces to do the fighting.
On Thursday, the top general in the US said the country’s intervention in Iraq could extend further.
General Martin Dempsey, chairman of the Joint Chiefs of Staff, said the role of calling in air strikes, which would put troops nearer the front lines, remained a future option.
And he raised the possibility of establishing a network of US training hubs in northern Iraq.