Dana Shell Smith announced the move a week after several Gulf states cut diplomatic ties with the monarchy in Doha, citing concerns over their financial ties to Islamist groups including the Muslim Brotherhood.
Saudi Arabia, Egypt, The Maldives, United Arab Emirates, Libya, and Bahrain won praise from Mr Trump for coordinating the anti-Qatari effort.
The President claimed foreign leaders had singled the country out for funding “radical ideology”, prompting criticism over his failure to address similar allegations levelled at his Saudi allies.
Ms Smith, a long-standing member of the US foreign service, has not indicated whether the ongoing crisis or the Trump administration played any part in her move, which the US State Department insists is “part of the normal rotation of career diplomats throughout the world”.
However when Mr Comey was fired on 9 May she tweeted: “Increasingly difficult to wake up overseas to news from home, knowing I will spend today explaining our democracy and institutions.
“Diplomats explain & defend our political system.Can be tough when partisan acrimony so high, but there is still no greater country. #USA.”
Ms Smith – who was appointed as the head diplomat in Doha by former President Barack Obama three years ago – has since tweeted that “Qatar is a strong partner in combating terrorist financing”, contradicting the US President’s public claims that the country is “a funder of terrorism at a very high level”.
Egypt has long thought Qatar’s support of Islamist groups Muslim Brotherhood was dangerous for their country.
Saudi Arabia also re-ignited tensions over Doha’s alleged support for Iran, which they claim could act to destabilise the region.
Last week Secretary of State Rex Tillerson asked that the nations in the anti-Qatari effort “ease the blockade against Qatar” and requested that Doha be “responsive” to its neighbours’ concerns over terror financing.
However, just hours later Mr Trump applauded the coalition and raised the possibility that the cutting of ties was due to his urging that Middle East countries more effectively address financing terrorists during his Riyadh trip.
Ms Smith re-tweeted Mr Tillerson’s comments but not the President’s tweets.
The US agreed to sell Qatar $12bn (£9.4bn)-worth of fighter jets just days after President Trump accused the country of being a sponsor of terrorism.
The deal was signed off by the US Defence Ministry and reportedly included 36 F-15 combat aircraft.
Two days before she left her job Ms Smith retweeted a post by Meshal Hamad al-Thani, Qatar’s ambassador to the US, which said the deal would create 60,000 new jobs in 42 states.
The Pentagon claimed the sale would increase security cooperation between the US and Qatar.
Qatar remains the home of some 10,000 American troops at a major US military base. So far, the dispute between Doha and nations led by Saudi Arabia has yet to shake that partnership, though cracks are showing in the responses from the US administration.