Khan, who has ambitions to become Pakistan's next prime minister, said in a Twitter post on Wednesday that the Trump administration was making Pakistan a scapegoat to cover Washington’s failure in neighboring Afghanistan.
"Pakistan has now suffered the ultimate insult (by) being made the scapegoat for US failures in Afghanistan," Khan said.
Trump said in his first tweet of 2018 that Washington had "foolishly given Pakistan more than $33 billion in aid over the last 15 years."
"They give safe haven to the terrorists we hunt in Afghanistan, with little help. No more!" wrote the US president on Monday.
Washington has long accused Islamabad of allowing the Haqqani network, which is an affiliate of the Taliban militant group, to operate relatively freely in Pakistan's porous border regions to carry out operations in Afghanistan.
Khan, however, mocked the Trump administration by challenging the American president to explain how "a couple of thousand or so (Taliban-allied) Haqqanis allegedly in Pakistan are supposed to be the cause of why the most well-equipped military force in history ... cannot succeed" in Afghanistan.
Pakistan's famous cricket star-turned-opposition leader, Khan also criticized Islamabad's participation in the so-called war on terror led by Washington.
"The lesson to be learned by us is never to be used by others for short term paltry financial benefits ever again," Khan said.
On Wednesday, former Pakistani Prime Minister Nawaz Sharif also said his country should end its dependence on aid from the US.
Sharif called Trump's tweet "non-serious" and "regrettable" and said the heads of state should keep international norms and diplomatic rules of engagement in mind when addressing other states.
At a top security meeting on Tuesday, Pakistan's civilian and military leadership angrily dismissed the threats by Trump to cut off aid as "completely incomprehensible." The "recent statements... by the American leadership were completely incomprehensible as they contradicted facts manifestly," read a statement issued by the prime minister's office after a meeting of the National Security Council. Trump's comments "struck with great insensitivity" and "negated the decades of sacrifices made by the Pakistani nation."
The US president's latest tweet comes following an increasingly tense back-and-forth between Washington and Islamabad. Relations between the two sides have taken a nosedive under the Trump administration. Washington has confirmed it will withhold $255 million in US military aid to Pakistan this year.
On Tuesday, the White House press secretary, Sarah Huckabee Sanders, told reporters to expect more details on specific actions against Pakistan over the next day or two.
Successive US governments have criticized Pakistan for links with the Taliban and for harboring slain al-Qaeda leader Osama bin Laden.