The performer’s outburst represents the first direct call for Mr Trump’s death by a figure at the funeral, which has already seen posters and graffiti demanding the killing of both the US president and Israeli Prime Minister Benjamin Netanyahu.
All of this is unfolding even as Tehran continues to negotiate with Washington over a permanent end to the conflict that has severely disrupted global energy supplies.
Poet Mohammad Rasouli drew calls of “Death to America!” and “Death to Israel!” from the assembled mourners.
Addressing the crowd, he drew loud cheers when, in reference to Mr Trump, he asked: “Why is the most b*stard man in the world still alive?”.
Sunday’s ceremony attracted a considerably larger crowd than the previous day’s proceedings.
Mourners dressed in black made their way to the site carrying banners and flags honouring Mr Khamenei, while also demanding Mr Trump’s killing as he delivered a speech in Washington marking the 250th anniversary of the founding of the United States.
“We’ve had tremendous success,” Mr Trump said, speaking of the American military. “You look at Venezuela, you look at Iran. We wiped it out, wiped out their military.”
The funeral for Mr Khamenei, who governed Iran for decades before he was killed aged 86 in a 28th February airstrike during the opening phases of the Iran conflict, could deliver a significant boost for the nation’s theocracy and its new supreme leader, his son Ayatollah Mojtaba Khamenei.
This proves crucial as Iran attempts to utilise its control over the Strait of Hormuz in discussions with the US regarding a lasting conclusion to the conflict, while apprehension persists that Israel might launch another offensive.
The funeral was postponed as the fighting continued and negotiations remain suspended until hostilities cease.