"The reason behind the foolish, very ugly, insolent and disorderly speech with cowboy and gangster wording... is their anger (and) desperation," Ayatollah Ali Khamenei said in reference to Trump and the US administration.
In remarks to a top clerical body, the Assembly of Experts, carried by his website, Khamenei described Trump and the US administration as "having no brains".
"The US president's remarks are not a source of pride for the American nation and the elite of that country should feel ashamed of... having such a president," Khamenei said.
Trump delivered a scathing verbal attack against Iran in his maiden speech to the UN General Assembly on Tuesday.
The US president referred to the Islamic republic as a "murderous regime" and a "depleted rogue state whose chief exports are violence, bloodshed and chaos".
He also called the nuclear deal between Iran and six world powers, including the United States, an "embarrassment" for Washington.
Tensions between Tehran and Washington have increased under Trump's administration.
But Tehran complains that the shadow of existing US sanctions have deprived it from the economic benefits it hoped to achieve from the deal.
The UN atomic watchdog has confirmed Tehran's compliance to the deal but the US administration says the "technical" adherence is not enough as long as Iran tests ballistic missiles and exerts influence in the region.
Trump said yesterday he has reached a decision on whether to recertify Iran's compliance with the deal to curb its nuclear programme, but did not reveal his intentions.
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