Jayewardene entered the University College, Colombo in 1926 where he attaining a distinguished academic record and showed a keen interest in sports. In 1928 he entered Colombo Law College and graduated as an advocate, starting his practice in the unofficial Bar, for a brief period. Jayewardene converted from Christianity to Buddhism in his youth.

Jayewardene did not practice law for long, however. In 1938 he became an activist in the Ceylon National Congress (CNC), which provided the organizational platform for Ceylon's nationalist movement (the island was officially renamed Sri Lanka in 1972). He became its Joint Secretary in 1940. He was elected to the colonial legislature, the State Council in 1943 by wining the Kelaniya by-election. During World War II, Jayewardene, along with other nationalists, contacted the Japanese and discussed a rebellion to drive the British from the island.

After joining the United National Party on its formation in 1946, he became Finance Minister in the island’s first Cabinet in 1947. He played a major role in re-admitting Japan to the world community at the San Francisco Conference.

Jayewardene's acute intelligence and subtle, often aggressive political skills earned him leading roles in government (1947 – 1956 and 1965 – 1970) and in opposition (1956 – 1965 and 1970 – 1977). In 1951 Jayewardene was a member of the committee to select a National Anthem for Sri Lanka headed by Sir Edwin Wijeyeratne. The following year he was elected as the President of the Board of Control for Cricket in Ceylon.

As the youngest Finance Minister, in D.S. Senanayake's government, Jayewardene struggled to balance the budget, faced with mounting government expenditures, particularly for rice subsidies. His 1953 proposal to cut the subsidies - on which many poor people depended on for survival - provoked fierce opposition and the 1953 Hartal campaign, and had to be called off.

By the late 1950s, the UNP struggled to deal with the rising force of the Sinhala nationalist Sri Lanka Freedom Party. Jayewardene pushed the party to accommodate nationalism and endorse the Sinhala Only Act, which was bitterly opposed by the island's minorities. Throughout the 1960s Jayewardene clashed over this issue with party leader Dudley Senanayake. Jayewardene saw how skilfully the SLFP had played the ethnic card, and felt the UNP should be willing to do the same, even if it meant losing the support of ethnic minorities.

No government gave serious thought to the development of the industry as an economically viable venture until the United National Party came to power in 1965 and the subject of tourism came under the purview of the Minister of State Hon. J.R. Jayewardene.

The new Minister Jayewardene saw tourism in a new dimension as a great industry capable of earning foreign exchange, providing avenues of mass employment, creating a manpower which commanded a high, employment potential in the world. He was determined to place this industry on a solid foundation providing it a 'conceptional base and institutional support.' This was necessary to bring dynamism and cohesiveness into an industry, shunned by leaders in the past, ignored by investors who were inhibited by the lack of incentive to invest in projects which were uncertain of a satisfactory return. The new Minister Hon. J.R. Jayewardene considered it essential for the government to give that assurance and with this objective in view he tabled the Ceylon Tourist Board Act No 10 of 1966 followed by Ceylon Hotels Corporation Act No 14 of 1966.

This was the beginning of a new industry ignored by the previous governments but given a new life by Minister J.R. Jayewardene. As a result today tourist resorts exist in almost all cities and today an annual turnover of over 500,000 tourists are enjoying the tropical climes and beautiful beaches of Sri Lanka not to mention the enormous amount of foreign exchange they bring into the country.

In the general election of 1970 the UNP suffered a major defeat, when the SLFP and its newly formed collation of leftist parties won almost 2/3 of the parliamentary seats. Once again elected to parliament J.R. Jayewardene took over as opposition leader and de-facto leader of the UNP due to the ill health of Dudley Senanayake. After Senanayake's death in 1973, Jayewardene succeeded him as UNP leader. He gave the SLFP government his fullest support during the 1971 JVP Insurrection (even though his son was arrested by the police without charges) and in 1972 when the new constitution was enacted proclaiming Ceylon a republic. However he opposed the government in many moves, which he saw as short sighted and damaging for the country's economy in the long run. These included the adaptation of the closed economy and nationalization of many private business and lands. In 1976 he resigned from his seat in parliament in protest, when the government used its large majority in parliament to extend the duration of the government by two more years at the end of its six year term without holding a general election or a referendum requesting public approval.

Jayewardene won a sweeping election victory in 1977 to become Prime Minister. Immediately thereafter, he amended the first republican constitution of 1972 and created the post of executive president. Provisions were included in it which made him President without an election. He swore as the President on 4 February 1978. He passed a new constitution on 31 August 1978 which came into operation on 7 September of the same year. It retained the Executive Presidency with drastic and unchecked powers, and, on its adoption into law, continued him as the first Sri Lankan Executive President. He moved the legislative capital from Colombo to Sri Jayawardanapura Kotte. He opened the heavily state controlled economy to market forces, which many credit with subsequent economic growth but also with greater divisions in society.

After the 1977 riots, the government made one concession to the Tamils; it lifted the policy of standardization for university admission that had driven many Tamil youths into militancy. The concession was regarded by the militants as too little and too late, and violent attacks continued.

Jayewardene moved to crack down on the growing activity of Tamil militant groups. He passed the Prevention of Terrorism Act in 1979, giving police sweeping powers of arrest and detention. This only escalated the ethnic tensions. Jayewardene claimed he needed overwhelming power to deal with the militants. He had likely SLFP presidential nominee Sirimavo Bandaranaike stripped of her civic rights and barred from running for office for six years, based on her decision in 1976 to extend the life of parliament. This ensured that the SLFP would be unable to field a strong candidate against him in the 1982 election, leaving his path to victory clear. This election was held under the 3rd amendment to the constitution which empowered the president to hold a Presidential Election anytime after the expiration of 4 years of his first term.

The UNP had obtained an overwhelming majority in the 1977 elections, and Jayewardene was loth to part with it. He therefore held a referendum to cancel the 1983 parliamentary elections, and allow the 1977 parliament to continue until 1989. He also passed a constitutional amendment barring from Parliament any MP who supported separatism; this effectively eliminated the main opposition party, the Tamil United Liberation Front.

Jayewardene said in Daily Telegraph, 11th July 1983," Really if I starve the Tamils out, the Sinhala people will be happy."

At first, the war went badly for the government, and the LTTE ended up in possession of Jaffna and most of the northern province. The army counter attacked with an offensive that threatened to retake the city, at the cost of many civilian casualties. Jayewardene had to halt the offensive after pressure from India pushed for a negotiated solution to the conflict. Jayewardene and Indian Prime Minister Rajiv Gandhi finally concluded the Indo - Sri Lanka Accord, which provided for devolution of powers to Tamil dominated regions, an Indian peacekeeping force in the north, and the demobilization of the LTTE.

The LTTE rejected the accord, as it fell short of even an autonomous state. The provincial councils suggested by India were the ones that did not even have powers of control over revenue, police, or government sponsored Sinhala settlements in Tamil provinces. Sinhala nationalists were outraged by both the devolution and the presence of foreign troops on Sri Lankan soil. An attempt was made on Jayawardene's life in 1987 as a result of his signing of the accord. Young, deprived Sinhalese soon rose in revolt, organized by the Janatha Vimukthi Peramuna (JVP) which was eventually put down by the government.

Jayewardene retired from politics in 1989; his successor Ranasinghe Premadasa was formally inaugurated on 2 January 1989.
Quite contrary to his predecessor, Sirima Bandaranaika, Jayawardena's foreign policy was aligned with American policies (earning him the nickname 'Yankie Dickie') much to the chagrin of India. Before Jayawardena's ascendency into the presidency, Sri Lanka had its doors widely open to its neighbourhood India. Jayawardena's tenure in the office restricted the doors to India a number of times; once an American company tender was granted over an Indian company tender.

On the economic front, Jayewardene's legacy was decisive. For thirty years after independence, Sri Lanka had struggled in vain with slow growth and high unemployment. Since Jayewardene's reforms, the island has maintained healthy growth despite the civil war.

On the ethnic question, Jayewardene's legacy is bitterly divisive. When he took office, ethnic tensions were present but the country as a whole was at peace. By the end of his tenure, Sri Lanka was facing not one but two civil wars, both featuring unprecedented levels of violence and brutality.

Though Jayewardene indeed did not take measures to stop the attack on Tamils, he was not opposed to them personally, only politically. He was not a racist but rather a man who knew how to exploit racism to win the majority.

Jayewardene married Miss Elina Bandara Rupasinghe in 1935, Ravindra "Ravi" Vimal Jayewardene is their only child, he was an Officer in the Sri Lanka Army and served as the Presidential Security Adviser. He was a notable marksman, pilot and the founder of the elite Special Task Force.