The news sent shock waves through the agency and has left career officials on edge, in part because of its abrupt nature -- taking place before their assignments end this summer and replacements have been found -- and in part because these officials help the secretary, a government novice, work with policy experts throughout the building.
While Tillerson was on his first overseas trip at the G20 in Bonn, Germany, his aides told the entire staff in the offices of the deputy secretary of state for management and resources and the State Department counselor that their current assignments were prematurely coming to an end, according to senior aides.
Staff who worked for the head of the latter division, State Department Counselor Kristie Kenney, was told Tillerson does not intend to keep her position. Kenney was one of the last remaining senior officials at the department, having served as an ambassador under Presidents Bill Clinton, George W. Bush and Barack Obama, and is expected to retire next week. An aide to Tillerson told CNN, "no decisions have been made" about scrapping the offices permanently.
Altogether, the move left some two dozen career foreign and civil service officers scrambling for reassignments within the department.
R.C. Hammond, a State Department spokesman now serving as a top communications adviser to Tillerson, said Friday morning that "the State Department is made up of a corps of very talented public servants. In some cases, we are redeploying people to new assignments where they can immediately put their talents to work."
Another Tillerson aide added, "The motivation was to move people way from idle roles into productivity."
The office of the deputy for management office handles long-term management and security issues as well as reviewing the budget, and was only created in 2011 by then-Secretary of State Hillary Clinton. Various secretaries have decided to appoint a close confidante as counselor to advise the secretary on policy, but it is a not considered a permanent office.
"They are being shifted now to new assignments," the aide said, noting that currently the employees do not have a principal official to staff. "The difference now is they are actually doing work. We think the American taxpayer will appreciate that."
President Donald Trump signed an executive order in his first days of office freezing federal hiring, so any vacant positions would be filled by existing employees.
Many career officials acknowledge the State Department has a bloated bureaucracy, and expected both offices to be part of a reorganization under Tillerson.
The staff positions are filled by career foreign service officers and civil servants as opposed to political appointees who serve at the will of the President. The career postings come with a start and end date that traditionally transcend any change in administration.
But Kenney's ouster and that of other staff on the seventh floor, where Tillerson sits, were described as abrupt and much sooner than expected.
The unusual move has left career employees on edge about Tillerson's reorganization of the entire agency and what it might mean for policy making.
"We keep hearing there is a plan to restructure but nobody knows what is going on," one senior career officer said. "Everybody is in the dark and it's causing a lot of anxiety."
These career officers consider themselves apolitical, often have regional expertise and serve as liaisons between the State Department leadership and the bureaus where policy expertise is centered.
The career officials voiced concern that Tillerson, a former CEO of ExxonMobil who has no previous government experience, either doesn't understand or appreciate the work of the State Department and won't be a forceful advocate for the agency with the White House.
On his first day in office earlier this month, Tillerson commended the thousands of career diplomats and civil service officers worldwide.
"I am honored to be serving alongside each of you," the 64-year-old Texan said. "State Department staffers in the field are not just conduits for policies and plans, you are our emissaries of our nation and the ideals we stand for. When people see you, they see America."
But he also struck a CEO-like tone at one point, saying he would be looking to reform the agency to make it more efficient.
"Change for the sake of change can be counterproductive, and that will never be my approach," he told them. "But we cannot sustain ineffective traditions over optimal outcomes."
The move comes on the heels of a purge last month of the top management leaders at the State Department.
The move left Tillerson with a huge hole at the State Department after the departure of the officials, who had a combined 150 years of institutional experience.
Kenney's departure leaves Tillerson, who came to the State Department with only a handful of aides, a bare-bones staff as he seeks to assert his role in the administration as America's top diplomat.
Chief among them is Tom Shannon, the former undersecretary for political affairs who served as acting secretary before Tillerson was confirmed. He is now serving as acting deputy secretary.
Elliot Abrams, Tillerson's top choice to be his deputy, was rejected by Trump after the President learned that the former deputy national security adviser had criticized him during the campaign. No replacement has yet been named.