President Barack Obama has asked Congress for 500 million dollars (£294 million) to strengthen more moderate Syrian rebels.
He made the request with the conflicts in Syria and Iraq becoming increasingly intertwined against the same Sunni extremist group.
Mr Obama's bid for the money for training and arms to the opposition in effect opens a second front in the fight against militants spilling over Syria's border and threatening to overwhelm neighbouring Iraq.
The train-and-equip mission would be overseen by the Pentagon and would mark a significant expansion of previous covert effort to arm the more moderate rebels who are fighting both the extremists and forces loyal to Syrian President Bashar Assad.
The president has long been reluctant to arm the opposition, in part because of concerns that weapons may fall into extremist hands.
But administration officials say the US has grown increasingly confident in recent months about its ability to distinguish the moderate rebels from the more extremist elements that include the al Qaida-inspired Islamic State of Iraq and the Levant, or ISIL, which has stormed into Syria and captured much of the northern part of the country.
The risk of US weapons and ammunition falling into the wrong hands appears to have only heightened now that ISIL has strengthened.
But Mr Obama's request to Congress appeared to indicate that tackling the crumbling security situation in Syria and Iraq trumped those concerns.
White House spokeswoman Caitlin Hayden said the military assistance "marks another step toward helping the Syrian people defend themselves against regime attacks, push back against the growing number of extremists like ISIL who find safe haven in the chaos, and take their future into their own hands by enhancing security and stability at local levels".
The Syria programme is part of a broader 65.8 billion dollar (£38.6 billion) overseas operations request that the administration sent to Capitol Hill.
The package includes money to help stabilise nations bordering Syria that are struggling with the effects of the civil war.
The president's cautious approach to Syria has come under increased criticism as the four-year civil war spills across the border into Iraq, with White House opponents arguing that Mr Obama's reluctance to arm the rebels gave ISIL the space to strengthen.
Like the more moderate Syrian rebels, ISIL is seeking to push Assad from power. The group seeks to carve out a purist Islamic enclave across both sides of the Syria-Iraq border.
With ISIL gaining strength, US officials say Assad's forces launched airstrikes on extremist targets inside Iraq on Monday.
The US is also considering targeted strikes against ISIL in Iraq, creating an odd alignment with one of Washington's biggest foes.
Mr Obama has ruled out sending US troops back into combat in Iraq. But he has dispatched nearly 600 US forces in and around Iraq to train local forces and secure the American Embassy in Baghdad and other US interests.
The White House has been hinting for weeks that Mr Obama was preparing to step up assistance to the Syrian rebels.
On May 28 he said that by helping those fighting for a free Syria, "we also push back against the growing number of extremists who find safe haven in the chaos".
Officials said the administration would coordinate with Congress and regional players on the specific types of training and assistance the US would provide the opposition.
One potential option would be to base US personnel in Jordan and conduct the training exercise there.
The Russian ambassador to the United Nations criticised Mr Obama's announcement, saying it would just drag out the conflict and that it was "moving things in the wrong direction".
Ambassador Vitaly Churkin said: "I think that this is an extremely big risk, and frankly a waste."
He told reporters at the UN that weapons and money could fall into the hands of ISIL.
He said the US and Russia, which has been Assad's most powerful international backer during the war, should be focusing on restarting political negotiations to end the conflict.