Career
JCT
He did though play seven matches and score six goals for the senior team JCT Football Club in the I-League. Pailan Arrows
During the summer of 2011 Singh signed with Pailan Arrows who were then Indian Arrows in the I-League. He scored his first and only goal for Pailan Arrows in the I-League on 28 April 2012 against HAL at the Bangalore Football Stadium in the 41st minute as Pailan ran out 2–1 winners.
Churchill Brothers
During the summer of 2012 Singh again moved on and signed for Churchill Brothers who are also of the I-League.
Mohammedan
Ajay moved back to Mohammedan to play in Calcutta Preimer League later that year before joining up with their squad for the 2015-2016 I-League 2nd Division. Lonestar Kashmir
Ajay Singh joined Lonestar Kashmir for 2015 I-League 2nd Division where he played 11 times and scored 11 times.