The inception of the AFLW in 2017 brought changes and difficulties; the club won two premierships in the newly established VFL Women's but had to rely on a council grant to raise the necessary funds to play in the increasingly professional competition and struggled against better-resourced opponents.

Guardian Australia notes Darebin's "long... reputation for developing star talent and setting the bar for the women's game", having produced AFLW players such as Katie Brennan, Daisy Pearce and Darcy Vescio.

A group of women from Northcote, inexperienced but wanting to play football, revived the club under the same name, training for a year at Fairfield Park with around 30 players.

In 1991, the Falcons rejoined the VWFL and began playing at McDonell Park, which Northcote Council (now City of Darebin) had made a women's sporting field.

After defeating the St Kilda Sharks in the semi-final, the club faced the Spurs in the grand final and recovered from a 36-point half-time deficit to win their first premiership by 13 points.

The site, located alongside the Merri Creek, was developed as part of an upgrade of sporting facilities for the 2006 Commonwealth Games, which were hosted in Melbourne.

[9] However, the Falcons still managed to progress to the grand final, setting up a rematch of the previous year's decider at Whitten Oval.

Despite the 48-point difference on the scoreboard, the match was still reported as a close and exciting game, characterised by skilled and contested play, pack marks and attacking forays effected by the teams' centre half-forwards.

[10] Kathy Zacharopoulos, a Darebin midfielder, won the Lisa Hardeman Medal as best on ground, while Alisha Habib, Julia Boyle and Moana Hope kicked multiple goals apiece for the Falcons.

It proved effective – the club continued its winning streak, defeating Diamond Creek again in the grand final at Northcote Park, 9.9 (63) to 4.7 (31).

[20] When the 2011 season began, Darebin's unbeaten run was finally broken by the St Albans Spurs in round 4, which defeated the Falcons by 48 points.

A number of Falcons played for Victoria at the AFL Women's National Championships in South Australia – O'Connor, Shevaun Hogan, Daisy Pearce, Anna Schwager, Samantha Smith and Natalie Wood.

[20] St Albans kicked eight of the first ten goals to enter half-time with a comfortable 33-point lead and continued to dominate in the second half, finishing 79-point winners (16.6 (102) to 3.5 (23)).

[26] The Falcons faced Diamond Creek in the grand final, again held at Coburg City Oval, where they started as favourites having only lost one match for the season.

[33] For the 2014 home-and-away season, the Falcons again went undefeated, facing Diamond Creek for the third consecutive year in the grand final at Coburg, which 1812 people attended.

[36] In June, Darebin received council funding for lighting upgrades at their home grounds – AH Capp and WH Robinson reserves.

[37] In the 2015 season, Darebin's two-season unbeaten run was stopped by University in round 2, but the Falcons went on to win the rest of their games for the home-and-away segment and won through to the grand final, against Diamond Creek once again.

Several Darebin players were affected by injury – O'Connor was unavailable after hurting her knee, while Brennan played with a stress fracture in her foot.

Shannon Egan stepped in to O'Connor's ruck role and Vescio played at centre half-forward to cover Brennan's change to a stay-at-home forward.

[41] The beginning of the AFLW proved troublesome for many VFLW teams; its commencement made elite-level women's football more professional – increasing the expected standards of clubs' staff, programs and venues.

[42] As a volunteer-operated club, it was also difficult for Darebin to compete with teams such as Geelong and Box Hill that were endowed with improved facilities and financial support by their wealthy AFL counterparts.

[44] The alternatives to departure were affiliating with an AFL club, which Darebin members wanted to avoid in the hope of maintaining their name and independence,[2] or finding external funding.

[55] A planned four-team 'super series', in which Darebin players had the chance to compete to audition for a place on an AFLW list, was then announced and also subsequently cancelled in August.

[56] Competitive VFLW football finally returned in February 2021, with Darebin's opening round match ending in a low-scoring 2-point loss to Williamstown.

[61] The remainder of the season could best be described as a year of two halves; after losing their next two matches, the Falcons hit form to record four consecutive victories and sit in fourth place on the ladder after seven rounds.

[62][63] Yet in the weeks to come, Darebin struggled against its more favoured opponents and ultimately failed to win another game for the rest of the season, finishing the year in eighth place.

[84] In 2015, a four-member club panel selected a Silver Jubilee team, made up of the best Darebin coach and players from their twenty-five years of football.