The French president scathed his US counterpart for “taking sides” in the dispute between Saudi Arabia and Iran.
And he urged Mr Trump to be patient and stick to the 2015 agreement between Iran and a number of world leaders in which Tehran pledged to curb its nuclear programme.
Mr Macron said: “We shouldn’t choose one side or another. Other great powers have.
“In the context of what we are living through, the 2015 agreement is what allows us to establish a constructive and demanding dialogue with Iran.”
Mr Trump visited Saudi Arabia earlier this year and has since accused their rivals Iran of having “fueled the fires of sectarian conflict and terror”
He said: “From Lebanon to Iraq to Yemen, Iran funds arms and trains terrorists, militias and other extremist groups that spread destruction and chaos across the region.
“It is a government that speaks openly of mass murder, vowing the destruction of Israel, death to America, and ruin for many leaders and nations in this very room.”
Mr Macron has taken a more delicate approach in his attempt to crack down on terrorism and those that sponsor terror.
He said today: “I want France to propose solutions and initiatives when there are new crises.
“The fight against Islamist terrorism is the priority of France’s foreign policy. France’s security is the main purpose of our diplomacy.”
Under Mr Macron, France’s focus appears likely to shift to intervention in areas where Washington sees little added value in doing so, such as Africa.
Mr Macron, who has some 4,000 troops spread across the West African Sahel region, said there would be a re-evaluation of troop needs in the coming weeks.
He said he would also continue to push for peace efforts between warring Libyan factions after bringing rival leaders to Paris in July.
Critics at home have said French policy on Syrian President Bashar al-Assad had in the past focused too much on calling for his eventual departure from power and backing his opponents leaving it ostracised in international talks.
He said: “Daesh [Islamic State] is our enemy. Restoring peace and stabilising Iraq and Syria is or priority. We must win the peace and change method.”
US officials said the missile was “likely an intermediate-range ballistic missile”, according to initial data.