None more so than from the African Union (AU), which said it was "frankly alarmed" by the President's statement before addressing America's dark history in relation to the continent.
"Given the historical reality of how many Africans arrived in the United States as slaves, this statement flies in the face of all accepted behaviour and practice," AU spokeswoman Ebba Kalondo said. "This is particularly surprising as the United States of America remains a global example of how migration gave birth to a nation built on strong values of diversity and opportunity."
She adds that "we believe that a statement like this hurts our shared global values on diversity, human rights and reciprocal understanding." African governments quickly found themselves in an awkward position. As top recipients of US aid, some hesitated to jeopardise it by criticising Trump, especially as his administration has sought to slash foreign assistance.
“Unless it was specifically said about South Sudan, we have nothing to say,” South Sudan government spokesman Ateny Wek Ateny told the Associated Press.
But South Africa's ruling African National Congress called Trump's comments “extremely offensive.” Deputy secretary general Jesse Duarte said developing countries do have difficulties but the United States itself has millions of people out of work or without health care, and “we would not deign to make comments as derogatory.”
South African opposition leader Mmusi Maimane called Trump's comments “abhorrent... The hatred of [Barack] Obama's roots now extends to an entire continent.”
African media outlets and the continent's young, increasingly connected population were not being shy.
“Well, that is the perfect definition of racism. That is all I have to say,” Kenyan entrepreneur Wangui Muraguri told the AP in his Nairobi office.
“Casual Friday at the White House is soon to include hoods and tiki torches at this rate,” South African media outlet Daily Maverick wrote.
Many on the world's second most populous continent reached for their smartphones, long-practiced in defending the vast and varied region from easy stereotypes. While 40 percent of the world's poor live in sub-Saharan Africa, according to the International Monetary Fund, the region also has billionaires, reality shows and a growing middle class.
Some quickly decided to own Trump's vulgar language or throw it back in his face.
“Good morning from the greatest most beautiful 'shithole country' in the world!!!” South African Broadcasting Corporation anchor Leanne Manas tweeted.
“As someone from South Shithole, Trevor is deeply offended by the president's remarks,” The Daily Show tweeted of its South African-born host, Trevor Noah.
In Kenya, East Africa's economic hub, political activist Boniface Mwangi pleaded: “Please don't confuse the (hash)shithole leaders we Africans elect with our beautiful continent.”
Trump's comments highlighted months of concerns about his lack of focus on Africa, including empty ambassadorial posts in key countries like South Africa, Egypt, Congo and Somalia. A list maintained by the Washington-based American Foreign Service Association says eight such posts are vacant.
Trump has expressed negative opinions about the continent in the past. “Every penny of the $7 billion going to Africa as per Obama will be stolen - corruption is rampant!” he tweeted in 2013.
The US President is hurting himself both at home and abroad with his latest comments, some Africans said.
“He has not only insulted Africans, he has also insulted African-Americans,” said Sylvester Odion Akhaine, associate professor of international relations at the Lagos State University in Nigeria. “Internationally, such language will deepen the isolation of the United States, a country that is already losing its global prestige.”
As outrage spread, the US government's own Africa Media Hub tried to put out the flames.
Without directly referring to Trump's statement, it tweeted that “US remains committed to working together w/Africans to realise the promise of a more peaceful, more productive, more prosperous 21st century Africa. US deeply respects the people of (hash) Africa & values its partnerships with them.”
The controversy is unlikely to end there.
The AP contributed to this report