Blues and Tigers went into the final pool fixture both undefeated and knowing victory would secure a home semi-final in the competition.
The home side impressed early on and opened up a 9-0 lead through the boot of fly half Gareth Davies before a double try burst before the break put the English side in control.
Leicester – cup champions in 2012 - then wrapped up the bonus point win in the second period and finished with six tries as depleted Blues suffered a catalogue of injuries.
And Blues – who won three out of four games in the competition – later bowed out of the competition as Northampton Saints took pole position in Pool 2 with a bonus point win over Wasps.
The game was played out in ice cold winds in the Welsh capital, but had all the heat and intensity of a typical Wales versus England encounter as both teams unloaded thundering tackles in the opening minutes.
Leicester centre Jack Roberts burst down field to show the talent in the visiting back line, while Miles Normandale – the try hero over Wasps last weekend – also showed his intent as he broke tackles and bulldozed into Leicester territory.
Davies opened the scoring with a well-struck penalty before slick handling from Leicester almost sent Thompstone over, with wing Owen Jenkins putting his body on the line to halt his run.
A brilliant break from Macauley Cook, from a superb flat defence breaking pass from Lucas Amorosino, split the Leicester defence open before they regrouped on halfway.
Wide men Amorosino and Jenkins looked lively in the opening quarter, as Blues looked to play with width and tempo whenever possible.
Centre Joaquin Tuculet saw a drop goal attempt drift wide, but the penalty was already awarded and back went play for offside and Davies made no mistake to double the lead.
The home forwards were going about their work with gusto with Rhys Williams, Cook and Craig Mitchell all offering themselves up as willing carriers.
Davies kicked deep into the Leicester 22 to set up another attack and yet another penalty at the breakdown gave the home fly half a simple three points for a deserved 9-0 lead at the midpoint of the half.
Visiting fly half Owen Williams got Leicester on the scoreboard after 22 minutes with a penalty of his own.
The Leicester defence was beginning to shut down any home attack and force the Welsh region back.
However, when they mounted an attack of their own it was Ellis Jenkins who brilliantly turned over the ball to win a penalty to a huge ovation.
Broken play saw Geraint Walsh pop a sublime pass out of the tackle and quick handling found Tuculet on the left wing, but his low kick ahead bounced off a Leicester man and ran dead.
Blues looked to be in control but suddenly it was Leicester who exploded into life with two tries in as many minutes.
First tighthead prop Fraser Balmain burrowed over after a series of drives and then from the restart the Tigers powered forward once more and wing Morris dotted down in the corner.
Blues made two half-time changes, with Lloyd Williams and Ben Roach introduced, as they looked to spark a second half comeback. But they were dealt a blow within minutes when Argentine Tuculet was forced off through injury.
Leicester looked to turn the screw as the home injury count mounted. They kicked to the corner and drove up close before scrum half David Mele spotted a gap, threw a neat dummy and ran over unopposed for a 22-9 lead.
The visitors were firmly in the ascendancy as a huge driving lineout saw Leicester make 30 metres and Harry Thacker peel off to win a penalty. Williams kicked to the corner and Leicester again powered for the line only to lose control when a bonus point try looked inevitable.
The away pressure, though, continued to build in the final quarter as Leicester chased a home semi-final.
Another penalty at the hotly contested breakdown allowed Tigers kick to the corner and this time the backs took possession and quickly whipped it down the line for Tommy Bell to score.
Blues tried to spark late on with Walsh and Jack Phillips combining down the left as the game opened up. But as the wide open spaces were created it was Tigers who struck with a clever cross field kick from Williams picking out Thompstone for a fifth try.
A knock on denied Owen Jenkins a consolation score in the corner and it was the East Midlanders who had the final word as a grubber kick from Williams evaded Cook and Thompstone pounced for his second of the game.
Timeline:
05m Davies p 3-0
15m Davies p 6-0
19m Davies p 9-0
22m Williams p 9-3
38m Balmain t Williams c 9-10
40m Morris t 9-15
50m Mele t Williams c 9-22
66m Bell t Williams c 9-29
74m Thompstone t Bell c 9-36
80m Thompstone t Bell c 9-43
Cardiff Blues: 15 Geraint Walsh (Lodge 76), 14 Owen Jenkins, 13 Joaquin Tuculet (Phillips 44), 12 Adam Thomas (Patchell 49), 11 Lucas Amorosino, 10 Gareth Davies, 9 Tavis Knoyle (L Williams 40); 1Thomas Davies (Thyer 59-62), 2 Rhys Williams (E Lewis 62), 3 Craig Mitchell (Filise 39-40, 56), 4 Miles Normandale, 5 Lou Reed (Roach 40), 6 Macauley Cook, 7 Ellis Jenkins, 8 James Sheekey
Replacements: 16 Ethan Lewis, 17 Brad Thyer, 18 Taufa’ao Filise, 19 Ben Roach, 20 Craig Lodge, 21 Lloyd Williams , 22 Rhys Patchell, 23 Jack Phillips