Kettering Town were originally formed in 1872, turning professional in 1891. The club graduated through twelve different leagues from 1892 until they became founding members of the Alliance Premier League in 1979. The club maintained its status in the top flight of semi-professional football until the 2000–01 season.

Many honours have found their way to Rockingham Road, winning the Midland Football League title in 1896 and 1900. The Southern League Championship was won on three occasions by the club, in 1928 and 1957 under Tommy Lawton and in 1973 under the guidance of Ron Atkinson. In the 1930s the club won the East Midlands League and in 1948 the Poppies became Birmingham League Champions.

In a Southern League game against Bath City on 24 January 1976, Kettering became the first British club to play with a sponsor's name printed on their shirts after signing a deal with local firm Kettering Tyres. The deal was brokered by chief executive and manager Derek Dougan. Four days later, The Football Association ordered the club to remove the slogan, but Dougan changed the words on the shirts to "Kettering T", and claimed that the T stood for "Town". Nonetheless, the FA ordered the club to remove the words, which the club did due to the threat of a £1,000 fine. Shirt sponsorship was eventually legalised within the English game in 1977. Kettering are also the first ever British team to have their initials on their ground's floodlights.

The club finished runners-up in the Football Conference in 1981, 1989, 1994 and 1998. The GMAC Cup, (the non-league, league Cup) was won in 1987 and the Poppies were runners-up in 1995, then known as the Bob Lord Trophy. County competitions have been won regularly by Kettering Town, with the Northants Senior Cup won on 28 occasions and the Maunsell Cup 13 times.

The FA Cup has brought success and publicity to Rockingham Road with the first round proper being reached on 41 occasions. In 1901 the club reached the last sixteen and in more modern times the Poppies reached the fourth round proper in the 1988–89 season and also the third round in 1991–92 only to lose to Kenny Dalglish's Blackburn Rovers. During the 1994–95 season the club made their debut live on Sky TV in a first round tie against Plymouth Argyle, soon followed by another appearance against Wrexham at Rockingham Road. As of 2013 (June) the Poppies had scored more goals than any other team in the FA Cup history, with 846 goals scored.

Wembley has been reached on two occasions before. The Poppies lost 2–0 to Stafford Rangers in the 1979 FA Trophy Final. More recently, the FA Trophy Final in 2000 saw the Poppies lose a closely fought final with Kingstonian 3–2.

Most recently, the club were narrowly relegated on the last day of the 2000–01 season which ended 30 years in the top flight of non-league football. The Poppies made a quick return to the Conference in the 2001/02 season winning the Southern Football League with a last-day victory at Tiverton Town under Carl Shutt, his first full season in charge.

Season 2005–06 was to be one of massive change at Rockingham Road. In October 2005 it was announced that long-serving Chairman Peter Mallinger was to hand over the reins to a consortium consisting of Imraan Ladak, Mick Leech and England legend Paul Gascoigne. Gascoigne was installed as manager, replacing Kevin Wilson, and ex-Arsenal stalwart Paul Davis was recruited as assistant manager.

The eyes of the world were on Gascoigne and the Poppies, and media interest was massive. However, for a variety of reasons, Gascoigne was only to remain in the job for thirty-nine days. Kevin Wilson was given his old job back, but only held onto it for two months as a run of one win in twelve games saw the Poppies slump into the bottom half of Conference North.

Chairman Imraan Ladak installed former Tamworth manager Mark Cooper as the new Kettering Town manager for the 2007–08 campaign. The club finished the season as Conference North champions, breaking several records along the way (including seven consecutive wins at the start of the season, 29 wins overall, and a divisional record of 97 points). As a result, the club was promoted to the Conference National. In the 2008–09 season, Kettering Town beat Lincoln City, Notts County and Eastwood Town to reach the fourth round of the FA Cup, where they faced Fulham at home. While twice pulling even with the Premier League squad and looking like they could possibly produce a draw late in the second half, they gave up two goals and ultimately lost the spirited match, 4–2.

Creditable finishes were achieved in the Blue Square Bet Premier League, until a disastrous move in 2011 from Kettering to Nene Park, the former home of Rushden and Diamonds, saw the Club in financial turmoil and relegation of two divisions followed a bottom of the table finish and the declaration of a CVA.

In February 2012 George Rolls took over control of the club from Imraan Ladak, although Rolls wasn't officially the Kettering Town owner he was involved in the day to day running of the club and John Beck was appointed Manager. On the 6th June 2012, George Rolls was suspended from football for five years after breaches of Football Association betting laws were proven, Rolls was also fined £10,000, and this led to the appointment of Ritchie Jeune as Chairman.

In September 2012, Imraan Ladak the owner of the Club assumed the role of Interim Chairman after a dispute. John Beck who had been appointed as Manager in June 2012 was asked to leave the premises just before a game against Bashley on 6th October. On 8th October, the lights were switched off at Nene Park and several games were postponed by the Southern League in order that the Club could find new investors. On 10th November 2012, Kettering recommenced their fixtures by playing Redditch United at Corby’s Steel Park with Alan Doyle as Caretaker Manager. Volunteers, led by Northampton businessman Ritchie Jeune, ran the Club in the absence of the majority shareholder and Director with the support of the Kettering Town (Poppies) Supporters Trust.

Thomas Baillie, the former head of the Youth set up, took over as Manager in February 2013 with Alan Doyle becoming Football Technical Director, and the experienced Dean Thomas arrived to become Assistant Manager. The inevitable relegation followed another season of turmoil and the club was placed in the Southern League Division One Central, with Dean Thomas assuming the Manager’s role and Thomas Baillie reverting to become Assistant Manager. The Poppies moved again to Latimer Park ground sharing with Burton Park Wanderers.

After a disappointing start to the 2013-14 Kettering whose Chairman was now Ritchie Jeune, went on a record 21 game unbeaten league run, following that up with 10 consecutive victories (9 in the league) in April to create a National record, ending the season in third place just, 2 points behind Champions Dunstable Town and losing to Slough Town in the Calor League Division One Central Play-off final in front of 2,331 at Latimer Park, the club’s most successful season in the last four campaigns. Sensationally though Dean Thomas stood down as manager of the club in mid-May 2014, leaving his assistant Thomas Baillie to return as joint manager along with Scott Machin.