He joined Levski in 1999 and won three consecutive titles. However, at this time he was used mainly as a substitute. He became a first team regular in 2003. In May 2006, Telkiyski won the Bulgarian championship with Levski for the fourth time. With Levski Sofia he reached 1/4 finals of UEFA Cup in 2005–06. Next season, Levski Sofia with Telkiyski, reached the group-stage of UEFA Champions League, becoming the first Bulgarian team that reached the groups.
On 3 January 2008, Levski and Hapoel Tel Aviv F.C. agreed on the transfers of Elin Topuzakov and Dimitar Telkiyski. The two players went to Israel. They signed their official contacts with Hapoel on 7 January 2007. Telkiyski chose to play with kit number 31. Both Topuzakov and Telkiyski made their debut for Hapoel Tel Aviv F.C. on 12 January 2008 against Hapoel Kfar Saba. Hapoel Tel Aviv lost the match 2–1. Telkiyski scored his first goal for Hapoel against Maccabi Herzliya, in a 3–2 win. In 2008, he won the Fan's player of the year award with his teammate Elin Topuzakov.
Amkar Perm
On 18 July 2009, Telkiyski arrived in Perm, to join FC Amkar on an 18-month deal. On 9 August 2009, he made his debut for the Russian side in the 1:0 away defeat against CSKA Moscow, coming on as a substitute for Nikolai Zhilyaev in the 83rd minute.
Levski Sofia 2nd Period
On 13 October 2009, Telkiyski returned to Bulgaria to sign a contract as a free agent with his former club Levski Sofia. He took the number 32. Mecho immediately started to help his team, assisting 3 goals for 4 matches. Dimitar ended the season with 16 appearances and 6 assistances. After couple of bad games and results, Levski however achieved qualifying for UEFA Europa League becoming 3rd in the final ranking. On 31 May 2010, Dimitar's contract was extended to summer of 2012. For the next 10/11 season, Dimitar changed his kit number to 8.
On 21 December 2011, Telkiyski signed with Chernomorets Burgas. He played only 4 games because heavy injury received on 21 March. And leaves the club in June, when his contract expired.
Lokomotiv Sofia
In June 2012 Telkiyski returned to Lokomotiv Sofia.
Telkiyski plays as a winger or as a central midfielder. He is famous with his free-kicks and penalty kicks. His strong foot is the right one. Mecho is a fast player, who can dribble very well, which often makes him hard for marking. He makes a lot of assists.
