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Hapoel Jerusalem Basketball Club was founded in 1935, and incorporated in 1943. It made its first appearance in the Israeli Basketball Premier League in 1955. Hapoel Jerusalem played in the first division most of the 1950s and 1960s, with notable players such as David Kaminsky. The following two decades had ups and downs, as Hapoel Jerusalem toggled between the first and second divisions.

In 1986, led by coach Simi Riger, the team advanced to the Premier League, after five consecutive years in the second division. Since then, Hapoel Jerusalem has remained in the Premier League. In 1996 and 1997, Hapoel Jerusalem won the Israeli Basketball State Cup, defeating Maccabi Tel Aviv in the finals, at the Yad Eliyahu Arena. The team was led by Adi Gordon.

In 2004, Hapoel Jerusalem won its first European title, the ULEB Cup (EuroCup), defeating Real Madrid in the final in Charleroi, Belgium.

In 2005, Israeli-Russian billionaire Arcadi Gaydamak purchased a large stake in the club. As a result, the team became stronger and signed four American players with NBA records – Tamar Slay, Horace Jenkins, Roger Mason, and Mario Austin, as well as Israeli star Meir Tapiro.

In 2007, Hapoel Jerusalem won its third Israel State Cup, defeating Bnei HaSharon. In early 2008 Hapoel Jerusalem came back from being 22 points down in the 4th quarter, to win its fourth State Cup, beating Maccabi Tel Aviv 93–89. In late 2008 it won its first Israeli Basketball League Cup, beating Ironi Nahariya.

In September 2009, oil tycoon Guma Aguiar became the team's sponsor and helped pay debts left by Gaydamak. On October 8, 2009, Hapoel Jerusalem beat Maccabi Tel Aviv in the Winner Cup finals, winning the club's second cup in a row.

One year after the mysterious disappearance of Guma Aguiar, in 2013 a new ownership group headed by entrepreneur Ori Allon took over. Guy Harel succeeded Dani Klein as general manager.

In April 2014, the New York Post and The Wall Street Journal reported that six-time NBA All-Star Amar'e Stoudemire might join Hapoel Jerusalem after his contract with the New York Knicks expired at the end of the 2014–15 NBA season. Stoudemire decided to retire from the NBA in July 2016.

Amar'e Stoudemire signed a two-year contract with Hapoel Jerusalem on August 1, 2016. In his first season with the team he helped it win the Israeli Basketball League Cup, defeating Maccabi Tel Aviv.

On June 20, 2014, the club signed coach Danny Franco. That same day, the club also signed season MVP Donta Smith. On June 25, 2014, the executive board of Euroleague Commercial Assets agreed to give Hapoel Jerusalem a wild card to compete for a spot in the EuroLeague qualifications.

On June 25, 2015, Hapoel Jerusalem won the Israeli Basketball Premier League Championship for the first time in their history, defeating Hapoel Eilat in the Final. On June 15, 2017, the club won the Israeli Championship for the second time, defeating Maccabi Haifa in the Israeli Final.