Weerakoon joined the Ceylon Civil Service in 1954 and was assigned as a cadet to the AnuradhapuraKachcheri as an understudy to the Government Agent of Anuradhapura, after which he spent a year in Jaffna where he learnt Tamil. After that he was transferred to Badulla but before he could assume duties, the order was withdrawn and he was sent to the Prime Minister's office. In 1953, he was appointed as the assistant secretary to the prime minister at the time, Sir John Kotelawela. He later became the secretary to the prime minister and continued after Solomon Bandaranaike became the prime minister in 1956. After his death, he served Wijayananda Dahanayake and Sirimavo Bandaranaike. Thereafter he worked for Dudley Senanayake although some in the UNP felt uneasy about his presence. After Sirimavo won the election again in 1970, he was transferred as Government Agent of Batticaloa and later Ampara, since he was deemed untrustworthy having conveyed information to the UNP Dudley Senanayake during Mrs. Bandaranike's previous regime. In 1976, he retired from his post to join International Planned Parenthood Federation, an NGO working in the area of family planning as its Secretary General. In 1977, J. R. Jayawardene appointed him as the Permanent Secretary to the Ministry of Plantation. In 1980, he joined the Prime Minister's office once again as secretary during the tenure of Prime Minister Ranasinghe Premadasa. Following the ethnic riots of 1983, he was appointed as Commissioner-General of essential services with wide-ranging administrative powers. In 1984 he rejoined IPPF as its secretary-general in London for one year, which entailed a great deal of travel from China to Africa to Mexico. Following President Premadasa's assumption of office he was appointed presidential advisor on international affairs during a period when Indo-Lanka relations were at their lowest, following the expulsion of the IPKF. After Premadasa's death, he continued as the advisor of his successor Wijetunge, and resigned in 1994 when Chandrika Kumaratunga became the president. After Ranil Wickremesinghe became the prime minister in 2001, Weerakoon was reappointed to his previous position of Secretary to the prime minister. He was an influential figure in Wickremesinghe's administration, especially in the peace process between the government and the Tamil Tigers. His memoir Rendering Unto Caesar was published in 2004 after Wickremesinghe's government was defeated.