The Minnesota representative described it as “an outrage” that Mr Miller, the driving force behind administration’s controversial immigration policies, had influence over the White House.
Her comments came following reports that Mr Miller had been personally lobbying the president to take Immigration and Customs Enforcement (ICE) in a “tougher direction”.
He was also the architect of Mr Trump’s so-called Muslim ban and policy of separating migrant children from their parents at the US border.
Ms Omar, one of the first two Muslim women elected to congress, tweeted: “Stephen Miller is a white nationalist. The fact that he still has influence on policy and political appointments is an outrage.”
Mr Miller is said to have been the impetus behind an ongoing shake-up of senior immigration officials at the Department of Homeland Security.
He is reported to have convinced the president to oust Kirstjen Nielsen, who resigned as homeland security secretary on Sunday, in part because she was trying to obey laws on treatment of refugees, granting of amnesty, and separation of families.
Last year a White House aide, speaking anonymously, claimed Mr Miller “actually enjoys” seeing pictures of migrant children detained at the border. They told Vanity Fair: “He’s a twisted guy … He’s Waffen-SS.”
Ms Omar’s tweet contained a link to a story about Mr Miller reportedly pushing Mr Trump to withdraw his nomination of Ronald Vitiello to be next ICE head due to his lack of support for fully closing the border between the US and Mexico.
The congresswoman’s post was quickly condemned by Donald Trump Jr, who replied: “I see that the head of the Farrakhan Fan Club, @IlhanMN, took a short break from spewing her usual anti-semitic bigotry today to accuse a Jewish man of being a ‘white nationalist’ because she apparently has no shame.”
Ms Omar has previously been rebuked by Democratic House speaker Nancy Pelosi for her “use of antisemitic tropes and prejudicial accusations about Israel’s supporters”.