In 1976, as part of the attorney general's 'Honors Program,' Holder joined the newly established public-integrity office of the 'Department of Justice' in Washington. Working in that position, he prosecuted public officials involved in government corruption at various levels. Some such personnel were the ambassador to the Dominican Republic, the treasurer of the state of Florida, a Pennsylvania-based judge, and an assistant U.S. attorney from New York.
He was a nominee of the then-president, Ronald Reagan, for the position of the associate judge of the ‘Superior Court’ of the District of Columbia. After assuming the post, Holder primarily headed civil and criminal cases. His tenure lasted for 5 years.
In 1993, President Bill Clinton nominated Holder for the position of the U.S. attorney for Washington, D.C, which the senate confirmed later that year. With this, he became the first African–American to preside over the largest U.S. attorney's office.
His 4-year tenure witnessed several progressive activities, with community outreach being the priority. He established a domestic violence task-force unit, brought in a community undertaking project, and introduced 'Operation Cease-Fire' to reduce gun crime.
Holder served on the board of trustees of 'The George Washington University' in 1996 and 1997. That year, President Clinton promoted him to the second-highest position of the 'Justice Department,' deputy attorney general. Holder was again the first African–American to serve in that post. In that capacity, he expanded his previous initiatives.
Holder presided over civil and criminal cases related to enforcement, litigation, and other administrative issues. He established 'Lawyers for One America' to prioritize the role of citizens in the legal process and to diversify the legal profession.
As the deputy attorney general, Holder prominently worked in the areas of budget and personnel issues such as solving disputes among department heads, briefing reporters on policy initiatives, and working on national security issues. He also presided over significant investigations such as the 2002 case of bribery and corruption in the 'Winter Olympics' in Salt Lake City, the enactment of the 'Independent Counsel,’ and the murders of Matthew Shepard and James Byrd Jr.
Opposing the model introduced under President George W. Bush’s administration, Holder advocated civilian trials for terrorism suspects. ‘Republican’ lawmakers were against Holder's suggestion.
Holder ordered the investigation of the accusation of misconduct involving the New Orleans police department, during Hurricane Katrina.
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In 2001, Holder quit his office and began his private practice as a litigation partner with 'Covington & Burling' in Washington, D.C. There, he worked on civil, criminal, and investigative matters, along with domestic and international advisory issues.
Two of Holder's significant clients at the firm were 'Purdue Pharma' and 'Merck & Co., Inc.' (one of the largest pharmaceutical companies in the world). He was also part of the dog-fighting investigation of the 'National Football League' (against Michael Vick) and the case involving 'Chiquita Brands International,' the country's leading distributor of bananas, and its payment of “protection money” to the 'United Self-Defense Forces of Colombia' (AUC).
In March 2004, under the leadership of Illinois governor Rod Blagojevich, Holder and 'Covington & Burling' represented the 'Illinois Gaming Board' as a team of special investigators. The investigation was short-lived and was canceled on May 18, 2004.
After serving as the senior legal advisor for Barack Obama's 2007–2008 presidential campaign, Holder was appointed as the attorney general in Obama's administration. The senate confirmed his post in February 2009.
On March 27, 2009, he assumed duty at the 'Lisner Auditorium' of the 'George Washington University.'
Holder and ‘Republican’ legislators were pitted against each other once again during 'Operation Fast and Furious.'
In February 2011, Holder, on behalf of his legal department, announced that he would no longer defend cases related to the 'Defense of Marriage Act,' citing it unconstitutional. He argued that the prohibition of gay marriage did not adhere to strict scrutiny.
In May 2011, Holder testified before the ‘Congress,’ speaking on the legality of the operation that captured and killed Osama bin Laden. Holder maintained that killing Laden was legal. However, he failed to produce documents related to the operation. Hence, the ‘Republican House’ held Holder in contempt of the ‘Congress.’ With this, he became the first head of the ‘Justice Department’ to be held in contempt of the ‘Congress.’ However, he did not face any criminal prosecution.
Later that year, the 'House Judiciary Committee' declared an investigation into Holder's conduct and what he knew about 'Operation Fast and Furious' in his previous testimony.
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In 2012, the 'House Oversight and Government Reform Committee' cited Holder for contempt of the ‘Congress,’ as he did not respond to the committee's issue of a subpoena regarding the documents related to 'Operation Fast and Furious.'
On August 12, 2013, Holder, on behalf of the 'Justice Department,' launched the 'Smart on Crime' program at the ‘House of Delegates’ meeting of the 'American Bar Association.'
In September 2014, Holder announced his resignation, and attorney general. Loretta Lynch succeeded him in April 2015.
Holder returned to private practice at 'Covington & Burling' later that year. However, he continued to provide legal assistance in political matters, such as the opposition of the practice of gerrymandering.
In early 2016, Holder represented the South Africa-based telecommunications company 'MTN Group,' negotiating a fine that the government of Nigeria had imposed on the company.
In October 2016, ‘Politico’ announced Holder's appointment as the chairman of the 'National Democratic Redistricting Committee.' He assumed office the following year.
In October 2018, a Trump supporter named Cesar Sayoc was arrested in Florida for sending packages that were suspected of containing explosives, in an attempt to attack the president, Holder, and other top political figures. Fortunately, none of the devices detonated, and no injury was reported.
That year, Holder hinted at his probable presidential run in 2020.