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One image taken by New York Times photographer Eric Lee shows the liberal governor shielding her face from the cameras while flanked by Trump aides.
Whitmer, 53, took the folder away moments later - but looked deeply uncomfortable in other shots, with commenters saying she seemed embarrassed to be meeting a political foe.
Lee himself appeared to recognize the gravity of the shot and shared a link to it on his X account yesterday afternoon
Governor Whitmer's trip to Washington D.C. centered on discussions about tariffs and the aftermath of a severe ice storm, for which she sought a Presidential Emergency Declaration.
However, her office stated she was unexpectedly brought into the Oval Office during President Trump's signing of executive orders and proclamations, leading to the photograph.
Online critics interpreted the image as Governor Whitmer's attempt to distance herself from the 78-year-old president, even though she was part of a bipartisan delegation advocating for Michigan.
'This looks so stupid and childish, that it needs to be printed & framed in the Oval Office,' one X user commented.
'Maybe she thought if she couldn't see Trump signing, the economy would magically fix itself in Michigan…' another said.
'Why didn't she just hold her head up high and express she was there for one reason only - the wellbeing of her state and no matter who is in office she is going to work with them for the better of her people? …like a normal governor should.' read a third comment.
Some observers contrasted her apparent discomfort in the Oval Office with her demeanor in previous public appearances.
'I need help understanding Democrat thinking. Gretchen Whitmer was embarrassed to be photographed standing in the Oval Office, but not embarrassed enough to do this,' another person added, referencing Whitmer's bizarre campaign video of her feeding Doritos to liberal podcast host Liz Plank.
Governor Whitmer, accompanied by Michigan State House Speaker Matt Hall and Trump's cabinet secretaries, stood near the Resolute Desk during the Oval Office appearance.
Trump used the occasion to announce investigations into Miles Taylor and Christopher Krebs, both individuals who had opposed him during his first term.