On 27 May 1936, five days after being registered as an airline, its first service began between Baldonnel Airfield in Clondalkin, Dublin and Bristol (Whitchurch) Airport, the United Kingdom, using a six-seater de Havilland DH.84 Dragon biplane (registration EI-ABI), named Iolar (Eagle).

Later that year, the airline acquired its second aircraft, a four-engined biplane de Havilland DH.86 Express named "Éire", with a capacity of 14 passengers.

[17] In 1937, the Irish government created Aer Rianta (now called Dublin Airport Authority), a company to assume financial responsibility for the new airline and the entire country's civil aviation infrastructure.

The airline's services were curtailed during World War II with the sole route being to Liverpool or Barton Aerodrome Manchester depending on the fluctuating security situation.

[24] The airline entered the jet age on 14 December 1960 when it received three Boeing 720 for use on the New York route and the newest Aer Lingus destination Boston.

[29] In September 1979, Aer Lingus became the first European airline other than Alitalia to be used by Pope John Paul II, when he flew aboard a specially modified Boeing 747 (EI-ASI or St. Patrick) from Rome to Dublin and later from Shannon to Boston.

As a result, it weathered the storm and returned to profit, largely through lowering the airline's cost base, updating the fleet with modern Airbus equipment and developing new routes to mainland European destinations.

[32][33] In preparation for the commercial flotation of Aer Lingus on the Dublin stock market, the Irish government agreed to abolish the Shannon Stopover from the end of 2006 in stages.

From Autumn 2007, Aer Lingus commenced direct flights to Orlando, San Francisco and Washington, D.C.-Dulles, facilitated by the arrival of two new Airbus A330 aircraft in May 2007.

[48] In October 2009, newly appointed Chief Executive Christoph Mueller announced a radical cost-cutting plan that would lead to the loss of 676 jobs at the company and see pay and pension reductions for those being retained.

Four aircraft were based there beginning April 2009, serving eight destinations that included Dublin, Faro, Knock, Málaga, Munich, Nice, Vienna and Zürich.

[citation needed] On 8 January 2010, due to the weak demand in air travel, Aer Lingus announced that it was to reduce the number of aircraft based at Gatwick from five to three.

[61] He was replaced by German-born Christoph Müller (alternative spelling "Mueller"), former head of TUI Travel and Sabena, who joined Aer Lingus on 1 October 2009.

Mueller indicated that Aer Lingus intended to reposition itself again, moving away from head-to-head competition with Ryanair in the low-cost sector to a more hybrid model with a stronger emphasis on service.

[69] On 27 February 2013, the European Commission blocked the third attempt by Ryanair to take over Aer Lingus, stating that the merger would have damaged consumers' choice and resulted in increased fares.

Aer Lingus supplied on a wet lease agreement four Airbus A320-214 aircraft (painted in Virgin's colours but under Irish registration[32]) as well as crew for these services, which operated from London Heathrow to Aberdeen, Edinburgh and Manchester.

[75] On 24 March 2021, Aer Lingus announced the launch of four new routes from Manchester Airport; New York John F Kennedy and Orlando from 29 July 2021, Barbados from 20 October 2021 and Boston from summer 2022.

On 25 February 2020, Aer Lingus noted it had been advised by the Department of Foreign Affairs that travel restrictions were being placed on several Italian towns within Italy's Lombardy region as a result of an outbreak of COVID-19 there,[84] however stated all flights would continue to operate,[84] further advising all flights operated would continue to comply with guidelines locally from the HSE as well as from the WHO and EASA.

[84] On 28 February, Aer Lingus had been informed that a passenger had travelled with COVID-19 on a service from Milan-Linate to Dublin[86] and that it was cooperating fully with the HSE and Department for Foreign Affairs.

[90] Aer Lingus subsequently announced network-wide reductions[91] which eventually saw its network of flights reduced by 95%,[92] the airlines plan for its biggest summer schedule within its history was scuppered as a result of what became a global pandemic.

[96] The airline subsequently entered into talks with trade unions about changes to work practices and proposed job cuts,[97] Aer Lingus CEO Sean Doyle commented that it would take years for the aviation industry to recover.

[97] Aer Lingus later confirmed it was seeking further temporary pay cuts and changes to work practices in a cost saving exercise,[98] advising that its 2021 schedule would be at least 20% lower than planned.

[98] Job cuts were confirmed later that month, those holding temporary contracts were made redundant[99] and cabin crew based in Shannon were informed that they would be temporarily laid off as the airline was not operating services from there.

[102] The airline stated on 15 June, that if acceptance was not agreed by 6pm that evening, it would withdraw its offer and implement them unilaterally with a 70% cut to employees' wages excluding pilots.

[103] As the deadline passed the airline initiated the action to implement the changes angering Trade Unions representing the majority of Aer Lingus employees.

[104] In June 2021, the airline said it wanted to freeze workers' pay for five years while it is proposing sharp cuts in rates paid to new cabin and crew staff.

[citation needed] Stobart Air was placed into liquidation in June 2021; Aer Lingus and BA CityFlyer stepped in to operate the routes on a temporary basis.

The union concessions that arose from the negotiations were detrimental to the airline's image however; by 2003 the wage freeze had been lifted and there were 3,800 voluntary redundancies with no forced layoffs.

The airline said that its head office building, which was stated by the International Business Times to require refurbishing, was too large for the company's needs following the "Greenfield" cost reduction programme.

[149] In January 2017, Aer Lingus announced its intention to finalise an order for eight A321LR twinjets to develop thinner transatlantic routes which cannot be operated profitably and fuel efficiently using A330s.