Ajagun is a youth product of the Nigerian's Dolphins F.C.. On 28 August2013, Panathinaikos announced Ajagun signed a contract for four years with the club. On his debut with Panathinaikos, he scored against Platanias. On 30 July 2015, Ajagun helped Greek club Panathinaikos come from behind to beat visiting Club Brugge of Belgium 2–1 in a UEFA Champions League qualifying round. Panathinaikos fell behind in front of their fans after just 10 minutes, but they showed great character to come back and win with two goals one in each half. And that was after they had defender Sergio Sanchez sent off two minutes from halftime and also missed a penalty in the 34th minute. Ajagun was replaced in the 46th minute on account of the red card against his team. Former Nigeria youth star Abduljeleel Ajagun scored for his Greek side Panathinaikos in his first league game of the 2015–16 season as they beat Levadiakos 3–0. On 29 January 2015, Panathinaikos announced that 23-year-old Nigerian midfielder Abdul Ajagun will continue his career at Levadiakos on loan until the end of season. Ajagun was not in manager's Andrea Stramaccioni plans and his departure will free a foreigner's position, in order for the Greens to complete Lucas Villafanez and Rodrigo Moledo's transfers. On 14 July 2016, Roda have announced the signing of former Nigeria youth international on season-long loan with a view to a permanent move. Ajagun, who played under the Miners boss Yannis Anastasiou will be hoping to make his mark in the Dutch elite division. On 15 April 2017, he scored a brace in a vital game against Sparta Rotterdam sealing a 3–1 home win in his club's effort to avoid relegation. On 7 May 2017, he scored at the last minute of the vital home game against Willem II sealing a 1–0 win but despite the win, the team from Kerkrade kept fighting Sparta Rotterdam and NEC for a chance to direct self-preservation, with one game remaining for the end of the season. On 5 July 2017, Ajagun will continue his career in Kortrijk on the coach Yannis Anastasiou's recommendation, as Panathinaikos announced officially. It has long been known to be official, that the Nigerian footballer was not in the plans of Panathinaikos coach Marinos Ouzounidis after returning from his long season loan to Roda. On 17 September 2017, he scored his first goal with the club in a 2–2 home draw against Anderlecht.