In 1989, his junior year, Virginia went to the NCAA championship game where it fought the University of Santa Clara to a 1–1 draw after 4 overtimes. While the teams wanted to continue to play, NCAA officials ended the game and declared the two teams co-champions. At the time there were no penalty kicks to end a tie. At the end of the season, Agoos represented the United States at the 1989 Maccabiah Games.
Upon graduating from college, Agoos played for the Maryland Bays of the A-League in 1991. On February 13, 1991, the Dallas Sidekicks of the Major Indoor Soccer League drafted Agoos with the second overall pick of the 1991 draft. He played in thirty games in the 1991–1992 season, scoring seven goals. In 1992, he left the Sidekicks to play full-time for the U.S. national team, but Dallas again selected him in a draft, this time the 1993 Continental Indoor Soccer League (CISL) draft, but he did not re-sign with the team. On June 26, 1994, after being cut from the U.S. roster for the 1994 FIFA World Cup, Agoos signed with the Los Angeles Salsa for the 1994 American Professional Soccer League season. The Salsa went to the playoff semifinals that season as Agoos was selected Second Team All League. In the fall of 1994, he moved to Germany, where he played for SV Wehen during the 1994–95 season. Agoos returned from Germany in 1995 to sign with Major League Soccer. While waiting for the new league's first season, Agoos served as an assistant coach to Bruce Arena at the University of Virginia. In order to create a league, MLS allocated various recognized players to each team. As part of this process, the league allocated Agoos to D.C. United where he joined Bruce Arena, the team's first coach. That year, Agoos won the first MLS Championship as well as the U.S. Open Cup. He followed it up the next year with his second MLS Championship. In 1998, DC United achieved its greatest accomplishment when it defeated Vasco de Gama to take the Interamerican Cup. Agoos then won his third MLS Championship with DC United in 1999. He spent 2001 through 2004 with the San Jose Earthquakes, and proceeded to win his fourth and fifth MLS Championships. Agoos was named MLS Defender of the Year in 2001 and earned a place in the MLS Best XI three times (1997, 1999, and 2001). In 2005, Agoos was named to the league's tenth anniversary All-Time Best XI. He was traded to the MetroStars after the 2004 season for a fourth round draft pick. In ten years in MLS, Agoos scored 11 regular season goals and added 25 assists in 244 matches. In 2005, he was named to the MLS All-Time Best XI, before retiring December 8, 2005.
Agoos made his debut with the United States national team on January 10, 1988, against Guatemala. His first national team goal came just three days later on January 13, 1988, also against Guatemala. He was the last member to be cut from the US squad for the 1994 FIFA World Cup and he burned his uniform upon hearing the news. He made the squad for the 1998 FIFA World Cup in France but did not play a single minute, in favor of David Regis. In the World Cup in South Korea/Japan at the age of 34, Jeff started the first three games (he scored an own goal to finish the scoring in the surprising win against Portugal) until he suffered a calf injury against Poland. He later missed the rest of the tournament. He was capped a total of 134 times for the U.S. Agoos earned his last cap against Wales on May 26, 2003.
Agoos was also a member of the 1992 Team USA Futsal team which won a silver medal at Hong Kong. He earned 10 caps and scored 2 goals with the futsal team.
Agoos was named as New York Red Bulls' Technical Director on September 28, 2006, serving under head coach Bruce Arena. He officially joined the Bulls organization on January 1, 2007. On January 7, 2008 he was promoted to Sporting Director.
^Goff, Steven. [Tuesday kickaround: USA-Paraguay, USA-Spain, Marcelo Bielsa, Jeff Agoos, Chad Ochocinco, TV listings "Tuesday kickaround: USA-Paraguay, USA-Spain, Marcelo Bielsa, Jeff Agoos, Chad Ochocinco, TV listings"]. Soccer Insider. Washingtonpost.com. Retrieved 29 March 2011.