The billboard, displayed at Enghelab Square on Tuesday, November 3, depicted Trump behind bars with his head bowed and carried a message pledging to unalive him.
The display marks a further escalation in anti-Trump rhetoric in Tehran, where billboards mocking the US president and demanding revenge have appeared regularly since the war began on February 28.
The conflict began with US-Israeli strikes that unalived Iran's Supreme Leader, Ayatollah Ali Khamenei.
The latest displays emerged amid renewed diplomatic efforts to bring Tehran and Washington to the negotiating table and prevent further fighting in a conflict that has spread across the region and contributed to rising global prices.
Trump, whose Republican Party faces crucial US midterm elections on Tuesday, has expressed optimism about a possible agreement with Iran, saying a deal "could happen".
Meanwhile, an open-air exhibition at Tajrish Square in northern Tehran featured paintings attacking the US president, including violent images portraying him injured and humiliated.
One of the paintings showed a bomb covering Trump's face, apparently referencing Belgian surrealist René Magritte's 1964 artwork, The Son of Man.
A life-sized replica of a prison cell also remained on display nearby, with an actor impersonating Trump spending the day inside. A screen beside the installation showed images of destruction allegedly caused by US strikes on Iran.
Iran has accused Trump of deliberately targeting civilian locations during the conflict, including a school and a wedding ceremony, resulting in dozens of fatalities, including women and children. The allegations have not been independently established in the report.
State-sponsored billboards and murals have been prominent features of Iranian public spaces since the 1979 Islamic Revolution. They are regularly used to commemorate allies, honour military figures and communicate political messages, particularly against the United States and Israel.
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