After a disappointing 2004 season Cunningham was traded to Colorado Rapids for a first-round 2006 MLS SuperDraft pick.

During the 2006 season Cunningham led the league in scoring with sixteen goals, winning the MLS Golden Boot.

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.

After the match, TFC coach John Carver said "I am thinking, ‘How did he score 99 goals?’ That's what I thought.’"[6] On August 8, 2008, Cunningham was traded to FC Dallas in exchange for a third-round pick in the 2009 MLS SuperDraft.

After Kenny Cooper left the club for 1860 Munich, Cunningham emerged as the team's go-to goal scorer.

[9] 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,[10] however no trade came to pass.

[13] At season's end, Columbus declined his 2012 contract option and he entered the 2011 MLS Re-Entry Draft.

In January 2012, Cunningham signed on with first division side and current runner up CSD Comunicaciones of Guatemala for the 2012 Torneo Clausura.

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

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.

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.