The club was founded in 1924 in Beit Jann, near Yavne'el, by Russian Jews affiliated with Hashomer Hatzair movement. Due to unemployment in Beit Gan, the club relocated to Afula. During its early days, Hapoel Afula played mostly in friendlies against the likes of Hapoel Haifa and in regional leagues, comprising clubs from the Northern and Haifa regions. After the Israeli Declaration of Independence, the club was re-established in 1951. At the summer of 1954, the club merged with neighboring football club, Hapoel Balfouria, which played at the time at the top flight of Israeli football, and played home matches in Afula. Since the 1957–58 season, while playing in Liga Alef, the second tier of Israeli football at the time, the club was officially known under its current name, although they were mentioned by the press in both Hapoel Afula and Hapoel Balfouria names. the club continued to play as Hapoel Afula, and the name of Balfouria was dropped. In the 1958–59 season the club finished bottom in Liga Alef, and went to play in the relegation play-offs. In spite the club finished the relegation play-offs in a perfect record against Hapoel Be'er Sheva, Hapoel Netanya and Maccabi Sha'arayim, they were eventually disqualified and demoted to Liga Bet for fielding ineligible player. The club played for 17 successive seasons in Liga Bet, until they were relegated to Liga Gimel at the end of the 1976–77 season. The club made an immediate return to Liga Bet, where they played up until the 1983–84 season, in which the club folded during the season. The club reformed in 2001, and reached Liga Bet in the 2002–03 season, where they finished runners-up in the North B division. In the following season, the club won that division and were promoted to Liga Alef. After 9 seasons in Liga Alef, the club finally managed to win promotion to Liga Leumit, when they won the 2012–13 season in Liga Alef North, by a margin of ten points, and made a return to the second tier of Israeli football after 54 years. In The 2013–14 season, the club reached the top play-off in Liga Leumit, and finished in the 6th place, an achievement which was bettered in the following season, after the club finished in the 4th place. In the 2014–15 Israel State Cup, the club eliminated top flight club, Maccabi Petah Tikva, in the Quarter-finals by away goals, and reached the Semi-finalsfor the first time in their history. However, in the Semi-finals, Hapoel Afula were hammered 0–7 by Hapoel Be'er Sheva in Teddy Stadium, Jerusalem. On 6 December 2017, the club won its first major trophy, after beating Hapoel Ramat Gan in the Toto Cup Leumit final.