What causes the average speed difference between the JFK to DEN flights and the JFK to LAX flights?
There is certainly a difference, but most of it definitely has a good explanation. Most of it is overhead such as taxi time that applies to both flights (almost) equally. This has a relative big impact on short flights.

The taxi out time for both flights will be about 27 minutes; JFK is not exactly known for its quiet taxiways. Both flights will add about 30 nautical mile for their departure route. 

Both flights will fly approximately great circle routes, probably less than 2% extra distance during cruise.

The LAX flight will typically do a straight in arrival, almost no extra distance there.

The DEN flight will typically do a full arrival, 30 NM extra distance there. 

The taxi in at LAX is 13 minutes on average, and 9 minutes at DEN.

Let's assume that both aircraft fly 460 knot true airspeed with 20 knots headwind during cruise, so 440 knots ground speed.

My estimates for the total flight times are then: 



JFK-LAX


GC distance 2150 n.m
Departure detour 30 n.m
Arrival detour 0 n.m (straight in)
Cruise detour 25 n.m
Total distance 2205 n.m
Taxi out: 27 minutes
Climb out: 60 n.m. @ 300 kts = 12 minutes
Cruise: 2085 n.m. @440 kts = 4 hour 44 minutes
Descent/Landing: 60 n.m @ 240 kts = 15 minutes
Taxi in: 12 minutes
Total time: 5h50 minutes
Margin: 10 minutes




JFK-DEN 


GC distance 1400 n.m.
Departure detour 30 n.m.
Arrival detour 30 n.m.
Cruise detour 15 n.m.
Total distance 1475 n.m.
Taxi out: 27 minutes
Climb out: 60 n.m. @ 300 kts = 12 minutes
Cruise: 1355 n.m. @440 kts = 3 hour 05 minutes
Descent/Landing: 60 n.m @ 240 kts = 15 minutes
Taxi in: 9 minutes
Total time: 4h07 minutes
Margin: 33 minutes