The request was contained in a legal brief filed Friday with the US court, whose nine justices will next month review whether or not to repeal the federal Defense of Marriage Act (DOMA), which bans marriage between homosexuals.
The document marks the first time a president has endorsed same-sex marriage rights before the Supreme Court.
According to the filing, the Defense of Marriage Act "violates the fundamental constitutional guarantee of equal protection" before the law stipulated by the US Constitution.
DOMA "denies to tens of thousands of same-sex couples who are legally married under state law an array of important federal benefits that are available to legally married opposite-sex couples," read the brief signed by US Solicitor General Donald Verrilli.
The case before the Supreme Court involves Edith Windsor, a lesbian who married in Canada in 2007 but whose spouse and partner of 40 years died. She was required to pay more than $360,000 in federal estate taxes because she was not considered married under DOMA.
The White House position, however, came under fire from Republicans in the House of Representatives.
In a brief filed Friday, they insisted they have a legal right to defend the law in the Supreme Court in the absence of a defense from the executive branch.
Last month, 10 US senators urged the court to uphold the act and not to recognize same-sex marriages from other states.
All of these senators had voted for the Defense of Marriage Act and in a friend-of-the-court brief, they said it was inconsistent for the Justice Department to have assured Congress the law was constitutional while it was being crafted in the mid-1990s only to raise questions now.
"The time to speak was in 1996, when Congress gave careful consideration to the need for DOMA," they argued.
The Obama administration's decision to challenge the law comes as little surprise. Obama has signaled on various occasions recently that he is that he is in favor of gay marriage.
During his second inaugural address last month, the president drew parallels between the struggle for gay rights and the Civil Rights movement of past decades.
"Our journey is not complete until our gay brothers and sisters are treated like anyone else under the law, for if we are truly created equal, then surely the love we commit to one another must be equal as well," Obama said.
He also drew a parallel between several watershed struggles in US history: the landmark Seneca Falls convention in 1848; the 1960s civil rights battles; and the Stonewall riots of June 1969, which are widely seen as having launched the gay rights movement.
Obama's also chose gay poet Richard Blanco to read a specially composed poem at his second inauguration.
Already during his first term in 2011, Obama abolished the Pentagon's "Don't Ask, Don't Tell" policy requiring military recruits to hide their homosexuality, or risk being expelled from the service.
In 2012, he became the first sitting US president to speak out in favor of gay marriage.
This past week, the Pentagon officially extended some military benefits to same-sex partners, but said services like medical coverage would not be offered to gay troops' spouses because of DOMA.
"One of the legal limitations to providing all benefits at this time is the Defense of Marriage Act, which is still the law of the land," Defense Secretary Leon Panetta said.
About 17,000 same-sex couples in the armed forces were affected by the decision, including 5,600 active duty service members.
The effect of the DOMA law is to ban gay marriage at the federal level. After victories in several local referendums however, it is now legal in nine out of 50 US states and in Washington DC.
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