In 1983, the Welsh League was reorganised to create a form of "premiership" for the leading clubs and Haverfordwest's facilities, administration and playing record secured their admittance.

In the nine years of existence of this National Division, Haverfordwest were out of the top six only once, but their way to the title was blocked by the powerful Barry Town side.

The 2020–21 season saw mixed fortunes for the club, recording a famous 2–1 home win over TNS, but narrowly missing out on a top 6 finish.

After a promising start to the 2022–23 season, a poor run of form due to a number of injuries to key players saw the team near the bottom of the Cymru Premier table, however a memorable 2–1 home win over high flying Connah's Quay in the final game of Phase One gave the team reason for optimism ahead of Phase Two.

During Phase Two, an upturn in form saw an end of season seven game unbeaten run lead the team to finishing in a Europa Conference League play off spot.

The play off final against Newtown A.F.C saw the league's highest attendance for the season, with 1,826 fans there to witness another penalty shootout.

Corey Shephard scored the winner for the second successive 4-3 penalty win for Haverfordwest, sending them into the first round of qualification for the Europa Conference League.

In June 2023 the club pulled off another impressive transfer coup, announcing the signing of former Chelsea and Fulham academy player, and England youth international Martell Taylor-Crossdale.

July 2023 saw another major coup, when the club managed to secure the signing of Maltese international Luke Tabone for an undisclosed fee from Gżira United.