Hoover did not have a birth certificate filed upon his birth, although it was required in 1895 in Washington. Two of his siblings did have certificates, but Hoover's was not filed until 1938 when he was 43.

Hoover obtained a Bachelor of Laws from The George Washington University Law School in 1916, where he was a member of the Alpha Nu Chapter of the Kappa Alpha Order, and an LL.M. in 1917 from the same university. While a law student, Hoover became interested in the career of Anthony Comstock, the New York City U.S. Postal Inspector, who waged prolonged campaigns against fraud, vice, pornography, and birth control.

He soon became the head of the Division's Alien Enemy Bureau, authorized by President Woodrow Wilson at the beginning of World War I to arrest and jail allegedly disloyal foreigners without trial. He received additional authority from the 1917 Espionage Act. Out of a list of 1,400 suspicious Germans living in the U.S., the Bureau arrested 98 and designated 1,172 as arrestable.

In August 1919, Hoover became head of the Bureau of Investigation's new General Intelligence Division, also known as the Radical Division because its goal was to monitor and disrupt the work of domestic radicals. America's First Red Scare was beginning, and one of Hoover's first assignments was to carry out the Palmer Raids.

In 1921, Hoover rose in the Bureau of Investigation to deputy head and, in 1924, the Attorney General made him the acting Director. On May 10, 1924, President Calvin Coolidge appointed Hoover as the fifth Director of the Bureau of Investigation, partly in response to allegations that the prior Director, william J. Burns, was involved in the Teapot Dome scandal. When Hoover took over the Bureau of Investigation, it had approximately 650 employees, including 441 Special Agents. Hoover fired all female agents and banned the Future hiring of them.

Hoover's biographer Richard Hack does not believe the Director was gay. Hack notes that Hoover was romantically linked to Actress Dorothy Lamour in the late 1930s and early 1940s, and that after Hoover's death, Lamour did not deny rumors that she had had an affair with him.

Hoover was credited with several highly publicized captures or shootings of outlaws and bank Robbers, even though he was not present at the events. These included those of Machine Gun Kelly in 1933, of Dillinger in 1934, and of Alvin Karpis in 1936, which led to the Bureau's powers being broadened.

Hoover realized that his job was then on the line, and he pulled out all stops to capture the culprits. In late July 1934, Special Agent Melvin Purvis, the Director of Operations in the Chicago office, received a tip on Dillinger's whereabouts that paid off when Dillinger was located, ambushed, and killed by Bureau agents outside the Biograph Theater.

In 1935, the Bureau of Investigation was renamed the Federal Bureau of Investigation (FBI). In 1939, the FBI became pre-eminent in the field of domestic intelligence, thanks in large part to changes made by Hoover, such as expanding and combining fingerprint files in the Identification Division, to compile the largest collection of fingerprints to date, and Hoover's help to expand the FBI's recruitment and create the FBI Laboratory, a division established in 1932 to examine and analyze evidence found by the FBI.

Some people associated with Hoover have supported the rumors about his homosexuality. According to Anthony Summers, Hoover often frequented New York City's Stork Club. Luisa Stuart, a model who was 18 or 19 at the time, told Summers that she had seen Hoover holding hands with Tolson as they all rode in a limo uptown to the Cotton Club in 1936.

Actress and singer Ethel Merman was a friend of Hoover's from 1938, and familiar with all parties during his alleged romance of Lela Rogers. In a 1978 interview she said: "Some of my best friends are homosexual: Everybody knew about J. Edgar Hoover, but he was the best chief the FBI ever had."

Hack further reported that, during the 1940s and 1950s, Hoover attended social events with Lela Rogers, the divorced mother of Dancer and Actress Ginger Rogers, so often that many of their mutual friends assumed the pair would eventually marry.

J. Edgar Hoover has been portrayed by numerous actors in films and stage productions featuring him as FBI Director. The first known portrayal was by an un-credited voice actor in the 1941 Looney Tunes short "Hollywood Steps Out". Some notable portrayals (listed chronologically) include:

In 1946 Attorney General Tom C. Clark authorized Hoover to compile a list of potentially disloyal Americans who might be detained during a wartime national emergency. In 1950, at the outbreak of the Korean War, Hoover submitted to President Truman a plan to suspend the writ of habeas corpus and detain 12,000 Americans suspected of disloyalty. Truman did not act on the plan.

The attorney Roy Cohn served as general counsel on the Senate Permanent Subcommittee on Investigations during Senator Joseph McCarthy's tenure as chairman and assisted Hoover during the 1950s investigations of Communists and was generally known to be a closeted homosexual. Cohn's opinion was that Hoover was too frightened of his own sexuality to have anything approaching a normal sexual or romantic relationship.

Hoover was 18 years old when he accepted his first job, an entry-level position as messenger in the orders department, at the Library of Congress. The library was a half mile from his house. The experience shaped both Hoover and the creation of the FBI profiles; as Hoover noted in a 1951 letter,

During the Lavender Scare, Cohn and McCarthy further enhanced anti-Communist fervor by suggesting that Communists overseas had convinced several closeted homosexuals within the U.S. government to leak important government information in exchange for the assurance that their sexual identity would remain a secret. A federal investigation that followed convinced President Dwight D. Eisenhower to sign an Executive Order on April 29, 1953, that barred homosexuals from obtaining jobs at the federal level.

In 1956, several years before he targeted King, Hoover had a public showdown with T. R. M. Howard, a civil rights leader from Mound Bayou, Mississippi. During a national speaking tour, Howard had criticized the FBI's failure to thoroughly investigate the racially motivated murders of George W. Lee, Lamar Smith, and Emmett Till. Hoover wrote an open letter to the press singling out these statements as "irresponsible".

The Apalachin Meeting of late 1957 embarrassed the FBI by proving on newspaper front pages that a nationwide Mafia syndicate thrived unimpeded by the nation's "top cops". Hoover immediately changed tack, and during the next five years, the FBI investigated organized crime heavily. Its concentration on the topic fluctuated in subsequent decades, but it never again merely ignored this category of crime.

Hoover worked to groom the image of the FBI in American media; he was a consultant to Warner Brothers for a theatrical film about the FBI, The FBI Story (1959), and in 1965 on Warner's long-running spin-off television series, The F.B.I. Hoover personally made sure Warner portrayed the FBI more favorably than other crime dramas of the times.

In 1960s, Hoover's FBI monitored John Lennon and Malcolm X. The COINTELPRO tactics were later extended to organizations such as the Black Panther Party, Martin Luther King, Jr.'s Southern Christian Leadership Conference, and others. Hoover's moves against people who maintained contacts with subversive elements, some of whom were members of the civil rights movement, also led to accusations of trying to undermine their reputations.

Hoover personally directed the FBI investigation of the assassination of President John F. Kennedy. In 1964, just days before Hoover testified in the earliest stages of the Warren Commission hearings, President Lyndon B. Johnson waived the then-mandatory U.S. Government Service Retirement Age of 70, allowing Hoover to remain the FBI Director "for an indefinite period of time." The House Select Committee on Assassinations issued a report in 1979 critical of the performance by the FBI, the Warren Commission, and other agencies. The report criticized the FBI's (Hoover's) reluctance to thoroughly investigate the possibility of a conspiracy to assassinate the President.

When Richard Nixon took office in January 1969, Hoover had just turned 74. There was a growing sentiment in Washington, D.C., that the aging FBI chief needed to go, but Hoover's power and friends in Congress remained too strong for him to be forced into retirement.

Skeptics of the cross-dressing story point to Susan Rosenstiel's lack of credibility (she pleaded guilty to attempted perjury in a 1971 case and later served time in a New York City jail). Recklessly indiscreet behavior by Hoover would have been totally out of character, whatever his sexuality. Most biographers consider the story of Mafia blackmail unlikely in light of the FBI's continuing investigations of the Mafia.

Hoover remained Director of the FBI until he died of a heart attack in his Washington home, on May 2, 1972. Operational command of the Bureau passed to Associate Director Clyde Tolson. On May 3, 1972, Nixon appointed L. Patrick Gray – a Justice Department official with no FBI experience – as Acting Director of the FBI, with W. Mark Felt remaining as Associate Director.

Hoover amassed significant power by collecting files containing large amounts of compromising and potentially embarrassing information on many powerful people, especially politicians. According to Laurence Silberman, appointed Deputy Attorney General in early 1974, FBI Director Clarence M. Kelley thought such files either did not exist or had been destroyed. After The Washington Post broke a story in January 1975, Kelley searched and found them in his outer office. The House Judiciary Committee then demanded that Silberman testify about them.

In 1979 there was a large increase in conflict in the House Select Committee on Assassinations (HSCA) under Senator Richard Schweiker, which had re-opened the investigation of the assassination of President Kennedy and reported that Hoover's FBI failed to investigate adequately the possibility of a conspiracy to assassinate the President. The HSCA further reported that Hoover's FBI was deficient in its sharing of information with other agencies and departments.

In his biography Official and Confidential: The Secret Life of J. Edgar Hoover (1993), Journalist Anthony Summers quoted "society divorcee" Susan Rosenstiel as claiming to have seen Hoover engaging in cross-dressing in the 1950s, at all-male parties.

The FBI Headquarters in Washington, DC is named the J. Edgar Hoover Building, after Hoover. Because of the controversial nature of Hoover's legacy, there have been periodic proposals to rename it by legislation proposed by both Republicans and Democrats in the House and Senate. For Example, in 2001 Senator Harry Reid sponsored an amendment to strip Hoover's name from the building. Reid said J. Edgar Hoover's name on the FBI building is a stain on the building. The Senate did not adopt the amendment.

In his 2004 study of the event, Historian David K. Johnson attacked the speculations about Hoover's homosexuality as relying on "the kind of tactics Hoover and the security program he oversaw perfected: guilt by association, rumor, and unverified gossip." He views Rosenstiel as a liar who was paid for her story, whose "description of Hoover in drag engaging in sex with young blond boys in leather while desecrating the Bible is clearly a homophobic fantasy." He believes only those who have forgotten the virulence of the decades-long campaign against homosexuals in government can believe reports that Hoover appeared in compromising situations.

Because Hoover's actions came to be seen as abuses of power, FBI Directors are now limited to one 10–year term, subject to extension by the United States Senate.

Hoover lived in Washington, D.C. for his entire life. He grew up near the Eastern Market in Washington's Capitol Hill neighborhood and attended Central High School, where he sang in the school choir, participated in the Reserve Officers' Training Corps program, and competed on the debate team. During debates, he argued against women getting the right to vote and against the abolition of the death penalty. The school newspaper applauded his "cool, relentless logic." Hoover stuttered as a boy, which he overcame by teaching himself to talk quickly—a style that he carried through his adult career. He eventually spoke with such ferocious speed that stenographers had a hard time following him.

Hoover's practice of violating civil liberties for the sake of national security has been questioned in reference to recent national surveillance programs. An Example is a lecture titled Civil Liberties and National Security: Did Hoover Get it Right?, given at The Institute of World Politics on April 21, 2015.

The Attorney General Robert H. Jackson left it to Hoover to decide how and when to use wiretaps, as he found the “whole business” distasteful. Jackson’s successor at the post of Attorney General, Francis Biddle, did turn down Hoover's requests on occasion.