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Formation to Wessex League (1946–1986)

The club was formed on 22 May 1946 by Derik Brooks and a group of friends in the Fleming Arms public house in Swaythling, Southampton and originally known as Swaythling Athletic, which then changed to Swaythling. The club began playing home matches firstly on Southampton Common and then at 'Westfield' in Swaythling. In 1950 they joined the Hampshire League. In keeping with their early progress, the club moved to a new ground at Ten Acres in 1957 – which remains their home to this day. In 1980 the club were renamed Eastleigh. Eastleigh were consistently one of the stronger teams in the top tier of the Hampshire League, Division One, in the early 1980s and they achieved their highest final position of 4th (three times: in 1982, 1984 and 1985.) Their first match in the FA Cup was a 2–1 success against Southern League side Poole Town in 1981. They went on to beat Melksham Town in the next round before succumbing 2–4 to another Southern League side, Dorchester Town.

Wessex League (1986–2002)

In 1986 Eastleigh F.C. were accepted as one of the founding members of the Wessex League and managed an 8th-place finish in their first season in 1986–1987. Eastleigh didn't manage a top seven finish until the 1995–96 season when a 4th-place finish was achieved, the first of six consecutive top-seven finishes. Paul Doswell joined the club in 2002 as manager and oversaw three successive promotions.

Rise up the leagues (2002–2005)

In 2002–03 they won the Wessex League and were promoted to Division One East of the Southern League. After finishing fourth in their first season, the club were promoted due to the formation of the Conference North and South taking clubs from the division above, and were transferred into the Premier Division of the Isthmian League.

The club finished third in its first season in the Premier Division, qualifying for the promotion play-offs. After beating Braintree Town 2–0 in the semi-final, they were promoted to the Conference South after a 2–1 victory over Leyton in the final. The club also won the Russell Cotes cup, beating Gosport Borough 3–1 in the final.

Conference South (2005–2014)

Eastleigh's first game in the Conference South was a 1–0 defeat to Hayes. Eastleigh finished their first season in the Conference South in a creditable eighth place. They narrowly missed out on a play-off place in the 2007–08 season coming sixth after a final day defeat at Thurrock (4–1). In 2008–09, they finished third, but lost to Hayes & Yeading United in the play-off semi-finals despite holding a 4–0 advantage at one stage during the first leg. In the 2009–10 season, Eastleigh reached the first round of the FA Cup for the first time narrowly losing to Barrow (2–1).

The ownership of the club changed in late 2011. On 26 November 2011, following a meeting of the board, it was announced that an offer from Bridle Insurance Limited for the majority shareholding of the club had been recommended for acceptance by the current shareholders. Bridle Insurance were then the primary sponsors of Oxford United. Chief executive Stewart Donald and chief operations officer Neil Fox would both come on to the Eastleigh board as directors, with Paul Murray remaining as chairman.

The takeover by Bridle Insurance was eventually confirmed when the club announced the company had acquired the club's shares on 1 February 2012. On 23 March 2012, chairman Paul Murray stood down from his post. Murray had formally stood down as chairman when the club was sold to Bridle Insurance, but had remained at the club in a non-executive chairman role. Mick Geddes was later appointed as his successor.

On 16 May 2012, Eastleigh won their first silverware for seven years, beating Totton 2–0 in the final of the Hampshire Senior Cup.

On Tuesday 11 September 2012, following three successive league defeats, the last 4–0 away to newly promoted side Billericay Town, the club announced, following a meeting between manager Ian Baird and Stewart Donald, that it had been agreed that Ian Baird would leave the club with immediate effect. Baird's replacement was announced the following day as ex-Stevenage Borough manager Richard Hill. Hill has also had spells assisting John Gregory at both Wycombe Wanderers and QPR, and Brian Little at Aston Villa. He has also been employed as assistant manager at Gillingham, Tranmere Rovers and Northampton Town.

Eastleigh came close to achieving promotion to the Conference Premier for the first time during the 2012–13 season, by making the Conference South play-offs through finishing 4th in the league. After initially losing the first leg of the semi-final against Dover Athletic at home 3–1, Eastleigh overturned this with a 2–0 away win in the second leg, so the match went to penalties, with Eastleigh losing 4–2. Eastleigh won the Conference South in 2013–14, sealing the title in front of a crowd of over 1,500 on 18 April 2014 when they beat Basingstoke Town 2–1 and achieved promotion to the Conference Premier for the first time in the club's history for the 2014–15 season.

Conference Premier / National League (2014–)

Eastleigh's first game in the Conference Premier was a 3–0 victory at Nuneaton Town. Their second game was their first ever live televised game on BT Sport; Eastleigh beat Aldershot Town 1–0 with an injury-time winning goal. The 2014–15 season also saw Eastleigh's second appearance in the FA Cup 1st round proper, where they reached the second round for the first time, beating Lincoln City in the first round with a last-minute goal. Eastleigh lost 2–1 at Southport in their first ever FA Cup second-round fixture. Eastleigh spent their entire first season in the top half of the league and enjoyed an unbeaten run at home until into the new year. As home form dipped their away form soared, the club picking up victories at Braintree, Chester and most notably Bristol Rovers, whom they beat 2–1. Eastleigh featured again on television with a convincing 4–0 home win over Macclesfield. Eastleigh eventually secured a 4th-place finish after five consecutive wins culminating in a 2–1 win at home to Kidderminster in front of a record crowd of 4,024. The playoffs proved a bridge too far for Eastleigh, who were beaten 2–1 at the Silverlake Stadium and 3–0 at Blundell Park by Grimsby Town to lose 5–1 on aggregate.

After a run of just one point from five games, on 23 September 2015, Richard Hill resigned as Eastleigh manager. Chris Todd was quickly appointed caretaker manager, and after three victories from four matches he was confirmed as the new manager on 15 October 2015. Eastleigh had a fine run of form under Todd and rose to third place in the league table by Christmas. Meanwhile, the club was gaining national coverage for its FA Cup exploits. Eastleigh travelled to Crewe in the 1st round and achieved their first ever giant killing, courtesy of a 1–0 win with a Ben Strevens penalty. In the second round, Eastleigh won 2–0 at minnows Stourbridge to record their first ever appearance in the Third round. On 9 January, Eastleigh drew 1–1 with Bolton. The game took place after much speculation it would be postponed, and sold out giving Eastleigh a new record attendance of 5,025. Ten days later Eastleigh travelled to Bolton and lost 3–2, having led 1–0 through a Joe Partington strike. As Eastleigh exited the FA Cup, league form dipped and they eventually finished seventh, missing out on a play-off place.

After just four games of the 2016–17 season, with Eastleigh languishing in 16th place, Chris Todd was relieved of his duties as Eastleigh manager. Ronnie Moore was appointed and enjoyed an unbeaten run to start his time at Eastleigh. On 4 October, Eastleigh beat Maidstone 3–0 to move up to 5th in the league after offering free admission for all, which attracted a crowd of 4,114. However Eastleigh's form dipped and Ronnie Moore left the club on 30 November with personal circumstances cited. Eastleigh promptly appointed Martin Allen, who had won the league with Barnet in 2015. Unfortunately, Allen had little success with Eastleigh and was sacked on 22 February after just two wins from fourteen games.

Whilst Eastleigh struggled in the league they again enjoyed success in the FA Cup. A first round home tie with Swindon Town was selected by the BBC for live coverage, and Eastleigh drew 1–1. Eastleigh won the reply 3–1 at the County Ground. Eastleigh again required a replay to beat FC Halifax Town in the second round triumphing 2–0 at the Shay having drawn 3–3 at the Silverlake. In the third round Eastleigh travelled to Brentford, followed by a record ever away following of nearly 1,500 fans. Eastleigh were 5–1 down at half-time and lost the game 5–1.

Richard Hill was brought in as director of football and in April 2017 was announced as the new Eastleigh manager for the 2017–18 season with Andy Hessenthaler as his assistant. Eastleigh had a poor start to the season and, on 18 December, Hessenthaler was appointed manager with Hill reverting to director of football. Eastleigh finished the season 14th, missing out on a top half placing for the second year in a row.

The summer of 2018 brought change off the field as Chairman Stewart Donald left for League One side Sunderland. His share of Eastleigh F.C. was transferred to Mark Jewell, the new chairman, and 3 other directors, Kenny Amor, Tom Coffey and Joanne Sprigg. In October 2018, following 4 victories manager Andy Hessenthaler left to join Dover Athletic. Ben Strevens was appointed as the new manager. Some good form in early 2019 contributed to Eastleigh finishing the season 7th and in the play-offs. Eastleigh faced a tie at Wrexham and won 1–0 in extra time through a superb Danny Hollands strike. In the semi-final, Eastleigh travelled to Salford. The game finished 1–1 after 120 minutes. Eastleigh led early in the penalty shoot out but eventually lost 4–3 after Chris Zebroski missed the decisive penalty.

The 2019–20 season was shortened by 9 games due to the COVID-19 pandemic. Eastleigh spent most of the season in the middle of the table, eventually finishing 16th. However, in the FA Cup, Eastleigh again reached the Second Round, having beaten Welling in the Fourth Qualifying Round (0-0, 4-2r) and Stourbridge in the First Round (2-2, 3-0r). Eastleigh faced Crewe Alexandra in a televised game at the Silverlake, drawing 1–1 with their League Two opponents thanks to a late equaliser from Southampton loanee Marcus Barnes. The Spitfires lost the replay at Crewe 3–1.

The 2020–21 season was behind closed doors due to the COVID-19 pandemic. Only two Eastleigh home games were available for fans to be at the stadium. The Spitfires finished 9th after losing 2–0 to Solihull Moors on the final day, denying them of a play-off place. During the season, Eastleigh modernised their badge. On 26 January 2022, Ben Strevens left Eastleigh by mutual consent before being replaced by Lee Bradbury. Eastleigh finished the season in 19th place.

In the 2022–23 season, Eastleigh finished in 9th place. On 2nd May 2023, Stewart Donald and his company SJD Leisure Holdings Limited completed the takeover of Eastleigh F.C. Donald has a controlling stake in the club of 85% becoming chairman once again with Tom Coffey assuming Vice Chairman position.

In the 2023–24 FA Cup, Eastleigh lost 3–1 to Newport County in a third round replay.