Professional

Upon graduating, Cunningham was selected ninth overall in the 1998 MLS College Draft by the Columbus Crew. As a rookie, he played in twenty-five games, mostly as a substitute, and tied the rookie record for goals (since broken by Damani Ralph) with eight. Cunningham became a starter in 1999 and held that role for several years. In 182 games for Columbus, he scored sixty-two goals and notched forty-three assists. He was named to the MLS Best XI in 2002, after scoring sixteen goals and adding five assists. After a disappointing 2004 season Cunningham was traded to Colorado Rapids for a first-round 2006 MLS SuperDraft pick.^[1] He left the Crew tied with Brian McBride for the all-time team lead in goals.

Cunningham finished the 2005 season with twelve league goals for Colorado. He scored twice against Fulham F.C. of the Premier League in the 2005 MLS All-Star Game. His showing in an all-star game against Real Madrid also earned good reviews, despite MLS's 5–0 loss. However, after the year Colorado shipped him to Real Salt Lake for Clint Mathis.^[2] Cunningham was seventh on the all-time MLS goalscoring list entering the 2006 season.

During the 2006 season Cunningham led the league in scoring with sixteen goals, winning the MLS Golden Boot. He also tied for the second-most assists in the league with eleven. Both totals (16 goals and 11 assists) set single-season records for the RSL franchise.

Cunnyingham with Toronto FC

On May 22, 2007, Cunningham was dealt to Toronto FC in exchange for Alecko Eskandarian and a first-round draft pick in the 2008 MLS SuperDraft.^[3] In Toronto, he wore the number 96 to represent the 96 MLS goals he had scored after the conclusion of his first season with Toronto FC.^[4]

Cunningham fell out of favor in his second season with Toronto FC, missing scoring a goal line ball that would have taken Toronto to the CONCACAF Champions League. After the match, TFC coach John Carver said "I am thinking, ‘How did he score 99 goals?’ That’s what I thought.’"^[5]

On August 8, 2008, Cunningham was traded to FC Dallas in exchange for a third-round pick in the 2009 MLS SuperDraft.^[6] He scored in his first match with FC Dallas on August 16, 2008, in a 2–1 loss to the Columbus Crew. It was Cunningham's 100th goal in MLS. Jeff played in 11 games with FC Dallas during the 2008 season scoring 5 goals.

Cunningham scored 17 goals in 2009, including four goals on August 1 against the Kansas City Wizards. After Kenny Cooper left the club for 1860 Munich, Cunningham emerged as the team's go-to goal scorer. He netted seven goals in five games in September, winning MLS Player of the Month and went on to win the 2009 MLS Golden Boot.^[7] Cunningham ended the 2010 season as the #2 career regular season MLS goalscorer with 132 goals.

After the 2010 MLS season FC Dallas declined Cunningham's contract option and Cunningham elected to participate in the 2010 MLS Re-Entry Draft. On December 15, 2010, Cunningham was selected by Columbus Crew in Stage 2 of the Re-Entry draft.^[8] Prior to Columbus re-signing him on January 28, 2011, Cunningham trained with Norwegian Premier League club IK Start and was rumored to be in talks for a permanent move,^[9] however no trade came to pass. His return to Columbus Crew was on February 22, 2011, in the second half of the Crew's CONCACAF Champions League quarter final game against Real Salt Lake.^[10] On July 7, 2011, Cunningham scored his 133rd career MLS goal to tie the league's all-time scoring record. The goal came in the 90th minute on a header to win a game against the Vancouver Whitecaps FC by a score of 1–0.^[11] He scored his 134th goal—a penalty kick in a 6–2 loss to Seattle Sounders FC—to claim the record outright on August 27.^[12]

At season's end, Columbus declined his 2012 contract option and he entered the 2011 MLS Re-Entry Draft. Cunningham was not selected in the draft and became a free agent. In January 2012, Cunningham signed on with first division side and current runner up CSD Comunicaciones of Guatemala for the 2012 Torneo Clausura.^[13]

After his release by Comunicaciones, Cunningham signed with NASL club San Antonio Scorpions FC on July 23, 2012.^[14]

As of November 29, 2013, Cunningham is on trial with Vicem Hai Phong F.C. of Vietnam's V.League 1.^[15]

International

In 1999, he played for Jamaica in a friendly international against Ghana.

Cunningham became a U.S. citizen in November 2001, and received his first cap for the United States national team less than a month later, on December 9, in a friendly against South Korea. He made his first start in a World Cup qualifier on September 7, 2005, against Guatemala. After a four-year absence from the national team, Cunningham was called up by Bob Bradley for friendlies against Slovakia and Denmark in November 2009. In a friendly against Denmark on November 18, 2009, he scored his first career international goal.^[16]

Club

As of September 25, 2012

International

As of February 16, 2012

International goals

#	Date	Venue	Opponent	Score	Result	Competition
01.	November 18, 2009	NRGi Park, Aarhus, Denmark	Denmark	1 – 0	1–3	Friendly

Club

Columbus Crew

• Lamar Hunt U.S. Open Cup: 2002
• MLS Supporters' Shield: 2004

FC Dallas

• Major League Soccer Western Conference Championship: 2010

Individual

• MLS Golden Boot: 2006, 2009
• MLS Best XI: 2002, 2006, 2009
• MLS 100 goals club
• MLS 50/50 Club^[18]