[17] When Howard was 14 and 15 years old, Peter Mellor, the former professional goalkeeper who was coaching for the United States Soccer Federation and writing the curriculum for the first U.S. Soccer National Goalkeeping License for coaches, saw the 14-year-old Howard in an Olympic Development Player camp, identified him as a star of the future, and placed him in the Olympic Development Program.

[21] Howard proved a star not only in soccer as a midfielder, but also on the basketball court, where he averaged 15 points per game and helped bring his team to the state finals in his senior year.

Howard was victorious in his MLS debut with the MetroStars on August 18, 1998, making five saves in a 4–1 win over Colorado at Giants Stadium (his only appearance of the year).

He also spent most of the international season with the United States Under-20 team, leaving the club to compete in the 1999 FIFA World Youth Championship in April and the 1999 Pan American Games in July.

Howard posted a 5–2–2 record with a 1.59 GAA in 2000, splitting time between the MetroStars and the United States Olympic team, also winning all three of his U.S. Open Cup starts that season.

Manchester United paid a US$4 million transfer fee to sign Howard in the middle of the 2003 MLS season, and he replaced Fabien Barthez as the club's first-choice goalkeeper.

In March 2004, however, Howard's poor parry handed a last minute goal to Porto, eliminating United from the UEFA Champions League.

[citation needed] After a period of rest, Howard reclaimed his starting position ahead of Carroll for the 2004 FA Cup Final, picking up a winner's medal.

Howard started the 2009–10 Premier League season with four consecutive clean sheets, including away to Portsmouth where he helped his team secure a 1–0 win.

[32] Howard saved a Jermain Defoe penalty in injury time to help his side draw 2–2 with Tottenham Hotspur on December 6, 2009.

[39] On March 2, 2013, Howard's run of 210 consecutive Premier League appearances dating back to September 2007 came to an end as he missed a game against Reading with a finger injury.

[42][43] On December 26, Howard was sent off in a 1–0 defeat to Sunderland, which ended Everton's hopes of remaining an entire calendar year unbeaten at home.

[46] On February 19, 2016, Everton manager Roberto Martínez confirmed Howard was expected to serve as the backup to Joel Robles.

[49] On November 6, 2016, Howard saved two penalty kicks – with a third also being sent off the crossbar – against the LA Galaxy to send Colorado to the Western Conference Championship.

[51] On March 4, 2020, Howard announced his return to professional soccer, signing a playing contract with Memphis 901 in the USL Championship, where he also served as sporting director and minority owner.

[53] Howard represented the United States under-20 national team at the 1999 FIFA World Youth Championship in Nigeria, playing in group stage victories over England and Cameroon, before a loss in the Round of 16 against Spain.

On May 2, 2006, Howard was named as one of three goalkeepers on the United States roster for the 2006 FIFA World Cup in Germany, but served as a backup to Kasey Keller.

Howard became the team's first choice goalkeeper under Bob Bradley and started in the 2007 CONCACAF Gold Cup final, a 2–1 win over Mexico.

Howard was the starting goalkeeper for the 2009 FIFA Confederations Cup, including the semi-final in which the United States upset Spain, then the number one-ranked team in the world.

[59] Howard's distribution to Landon Donovan led to the game-winning goal of the final group match against Algeria, giving the United States passage into the round of 16.

After Mexico defeated the United States to win the 2011 Gold Cup Final, Howard made a controversial statement regarding the post-match ceremony.

[62] On June 22, Howard was named man of the match for his display during the United States' 2–2 draw with Portugal;[63] his most notable save was a reaction stop to deny Éder, having previously diverted Nani's shot onto the post.

[50] However, following to national team's failure to qualify for the 2018 World Cup later that year, after a surprise 2–1 away defeat to Trinidad and Tobago on October 10,[71] he was no longer capped at international level.

[26] In 2014, the U.S. Tourette Syndrome Association described him as the "most notable individual with Tourette syndrome around the world"[76] when he was deemed a "Champion of Hope" for the "tremendous courage he displayed in sharing his story on an international platform, educating the public on a disorder that is so seldom talked about, and encouraging young people living with TS to speak out about their experiences".

[77] Howard's autobiography, The Keeper: A Life of Saving Goals and Achieving Them (ISBN 978-0-06-238739-4), was co-authored with Ali Benjamin and published in 2014.

[15] In the book, Howard says that his neurological makeup gave him an enhanced perception and an ability to hyper-focus that contributed to his success on the field.

[15] The New York Times book review said that "few are cooler or quicker than Mr. Howard" and that "the story is good, but reading it require[s] a certain tolerance for sports clichés".