New York Red Bulls Agudelo began his career with the
New York Red Bull Academy a member of the
U.S. Soccer Development Academy and quickly established himself as one of the more skilled prospects at the club. In 2009, he was offered a chance to join the junior team but decided to accept a trial with Colombian side
Millonarios in 2010. Although it was reported that he had signed with Millonarios, he returned to the United States to join Red Bulls during their pre-season. While with
Millonarios, Agudelo played with the youth side, including a match against
Independiente Santa Fe on January 17, which served as a tribute match to Brazilian great
Pelé. On March 26, 2010, Agudelo officially joined the New York Red Bulls. He made his professional debut on April 27, 2010, in a
U.S. Open Cup game against
Philadelphia Union. Agudelo made his MLS debut against
Real Salt Lake October 9, 2010, entering in the 85th minute in a match that ended in a scoreless draw. He scored his first professional goal on March 19, 2011, in the Red Bulls' 2011 MLS season opener, a 1–0 victory over
Seattle Sounders FC. In October, MLS listed Agudelo at no. 2 on its "24 under 24" list of best young players for 2011. As directed by US National team manager
Jürgen Klinsmann, that all off-season US MLS stars should train with European clubs, on November 16, 2011, Agudelo started a two-week training period with
VfB Stuttgart. On December 1, 2011, Agudelo started a similar two-week period at
Liverpool.
Chivas USA Agudelo was traded to
Chivas USA on May 17, 2012, in exchange for defender
Heath Pearce, allocation money, and future considerations. The latter was reported to be a portion of any transfer fee that Chivas USA receives from selling Agudelo. Following the
2012 Major League Soccer season, Agudelo was invited to train with Scottish club
Celtic. Following his training stint with Celtic, Agudelo joined
West Ham United for a training stint also. He scored four goals for Chivas in
2012 as they had a poor campaign finishing bottom of the Western Conference. Agudelo was listed by MLS at no. 13 on MLS' annual "24 under 24" list of best young players. Agudelo began the
2013 well, scoring against
FC Dallas and
Chicago Fire before he was transferred to the
New England Revolution on May 7, 2013.
New England Revolution Agudelo was traded to
New England Revolution in exchange for allocation money on May 7, 2013. Agudelo made his New England debut in a 2–0 win over
Houston Dynamo and he was credited with their second goal which was originally given as an own goal. He then scored against
Toronto FC and
Vancouver Whitecaps FC before being ruled out for a month with a knee injury. In August 2013 Agudelo began to attract interest from English
Premier League side
Stoke City. Agudelo returned from injury on August 17, against
Chicago Fire and scored a spectacular back-heel goal in a 2–0 victory. The strike was subsequently a finalist for MLS Goal of the Year.
Stoke City On August 9, 2013, it was announced that Agudelo had signed a pre-contract agreement with English club
Stoke City and will join the Potters on January 1, 2014, once his contract with the
New England Revolution has expired. However the move fell through after he was denied a work permit. Despite this, Stoke completed the signing of Agudelo on January 21, 2014, and loaned him out to Dutch side
FC Utrecht for the remainder of the
2013–14 season. He scored his first goal for Utrecht on February 6, 2014, scoring against
PEC Zwolle in a 2–1 defeat. Stoke re-applied for a work permit for Agudelo in May 2014 but were again unsuccessful. Following this Juan Agudelo had the option to join a team in Germany, but decided to head back to the States and continue his career with the USMNT and New England Revolution, where he felt his best and at home.
Return to New England On January 30, 2015, Agudelo re-signed with the New England Revolution after tweeting out "I am extremely happy to officially sign minutes ago and be back with the best teammates and coaching staff #NERevs". in the
2015 MLS Cup playoffs, he scored a "stunning" bicycle kick against
D.C. United to give the Revolution a 1–0 lead. In October, MLS listed Agudelo at no. 13 in its "24 under 24" list of best young players for 2015. In the
2016 season, Agudelo led the Revolution scoring, recording seven goals and five assists. He was listed as the 17th best young player on MLS' 2016 "24 under 24" list. He recorded a career-high eight goals in the
2017 season, and was named MLS Player of the Week for MLS match week 4 after recording a brace against
Minnesota United FC. On December 3, 2019, Agudelo was selected by
Toronto FC in Stage Two of the
2019 MLS Re-Entry Draft, however, they were not able to reach a contract agreement. Agudelo made his Miami debut in the club's first ever-match, a 1–0 loss to
Los Angeles FC on March 1, 2020. He scored his first Miami goal on July 8 in the
MLS is Back Tournament in a 2–1 loss to
Orlando City SC, and notched two more goals and in 14 total appearances for the club during their
inaugural campaign. Miami opted to decline his contract option following the 2020 season.
Minnesota United On March 2, 2021, Agudelo signed as a free agent with
Minnesota United FC on a one-year deal. He appeared 13 times for the club. .
Birmingham Legion On March 31, 2022, Agudelo signed with second-tier side
Birmingham Legion who play in the
USL Championship, rejoining
Tom Soehn and
Jay Heaps, who had both coached him while in New England. Agudelo contributed seven goals and five assists in his first season in Birmingham, and the club re-signed him prior to the
2023 season. He was named
U.S. Open Cup Lower Division Player of the Tournament for
2023, scoring three goals and recording a game-winning assist as the Legion reached the quarterfinals.
San Antonio FC Agudelo moved to USL Championship side
San Antonio FC on December 21, 2023, ahead of their upcoming 2024 season. ==International career==