Full-time score from The DenWith the fans in full voice The Lions were in no mood to relinquish the lead - or three points - and the final whistle was met as much by relief as delight at a job very well done.
And with the clock ticking towards the end of the 90th-minute, that man Henderson exchanged passes with Keogh before working his way into the left side of the area where he arrowed a shot past Bogdan into the bottom right corner.
Jackett then brought on Shaun Batt for Malone as The Lions went for broke. Debutant Beevers sent a header straight into the hands of keeper Bogdan late on as Jackett's men prised and probed in search of that winning goal.
Eagles, clearly frustrated by his penalty miss, clattered into Keogh just three minutes later and was perhaps lucky to escape with only a yellow card for a crude challenge.
Bogdan made a fantastic save to turn behind Henderson’s goalbound 25-yard free-kick behind as it headed towards the top corner and Malone fired a volley well wide from 20 yards before Jackett introduced Andy Keogh and Chris Taylor for Wood and Henry with 17 minutes remaining.
Millwall seemed to visibly grow in confidence and belief and, roared on by the crowd, pushed on in a bid to gain the upper hand once again.
And Eagles was guilty of an even worse miss just past the hour-mark when, having been tripped by Alan Dunne, he picked himself up, dusted himself down and then promptly fired the resulting penalty wildly over the bar - much to the delight of the home fans.
The Lions then had a lucky let-off when Eagles steered an effort wide of an empty net from a tight angle after Davies had picked him out with a cross from the right.
Trotter looked to have been impeded shortly after when he was sent tumbling in the area as he raced through to meet a long ball, but his appeals fell on deaf ears.
Bolton were handed a great opportunity to get back in the game a couple of minutes later when Liam Trotter fouled Mark Davies just outside the penalty area and up stepped Eagles to drill a low free-kick under the wall and beyond the reach of Forde to level things up.
Wood went close again three minutes after the restart after Henderson's neat ball had again set up Henry to provide the ammunition; on this occasion it was the reflexes of Bogdan that denied the Millwall man with a fine block.
In fact Chris Wood could have doubled Millwall's tally seconds before the break but headed a pinpoint Henry delivery agonisingly wide of the mark from close range.
Although The Lions went in 1-0 ahead at the half-way stage, they were indebted to the athleticism of keeper David Forde, who flung himself across goal to make a breathtaking save from Eagles, pushing his' piledriver over the bar for a corner.
At the other end Tyrone Mears failed to hit the target from 18 yards with a free-kick on the edge of the 'D' after Shittu had been penalised for a foul on Keith Andrews.
The Lions could have doubled their tally after 37 minutes when a neat move involving Henry and Henderson set up Scott Malone inside the danger zone, but his attempt to toe-poke the ball past Bogdan saw the ball sail harmlessly wide of the target.
Bolton had a penalty appeal turned down seven minutes later when former Lion Kevin Davies' strike appeared to hit the hand of left-back Jack Smith, although it did look more a case of ball to hand and play was waved on.
Bogdan then had to be alert to avert the danger as Henderson threatened, but there was little the keeper could do to prevent the prolific frontman from firing Millwall into a 17th-minute lead with a shot from just outside the area that took a deflection on its way into the back of the net past the wrong-footed stopper.
Shittu thought he had made the breakthrough in the opening six minutes with a firm header from James Henry's sixth-minute corner, but the effort was ruled out for a foul on keeper Bogdan.
Jackett handed a debut to defender Mark Beevers, barely 24 hours after joining on an emergency loan from Sheffield Wednesday, and he slotted in seemlessly alongside the outstanding Danny Shittu in the heart of the back four.
"We continue to create chances and all of our front players had good opportunities. The highlight today for, though, me was the relationship between the players and the fans. It was fantastic."
And manager Kenny Jackett was quick to praise the support of the home fans: "The win today made the last two performances and results away from home very good," he said.
Having recorded successive draws on their travels at Burnley (2-2) and Bristol City (1-1) in the past seven days, The Lions were looking to enjoy a little home comfort back in SE16 and record only a second home win of the season.
Roared on by the home crowd, Henderson scored his - and Millwall's - second in the dying seconds of normal time with a crisp angled finish beyond the reach of visiting keeper Adam Bogdan.
Eagles then wasted a glorious opportunity to fire the visitors ahead blasting a 61st-minute penalty yards over the bar after Alan Dunne had been penalised for a foul on the former Burnley man.
In a cracking match that saw The Den faithful play their part with some full and fine vocal support, Henderson opened the scoring after 17 minutes only for Owen Coyle's Trotters to level on 50 minutes courtesy of a Chris Eagles free-kick.
Darius Henderson bagged a dramatic 90th-minute winner as Millwall recorded their first victory in six games against Bolton Wanderers.
Forde, Dunne, Smith, Abdou, Shittu, Beevers, Malone, Trotter, Henderson, Wood, Henry. Subs: M.Taylor, Wright, Racon, Batt, Mkandawire, C.Taylor, Keogh. Bogdan, Mears, Mills, Eagles, Andrews, Ngog, Knight, Davies, Warnock, M.Davies, Spearing. Subs: Ream, Afobe, Ricketts, Sordell, Pratley, Lonergan, Yong Lee.