There really is no such thing as a flute that is in tune. Certainly, flutes can be played in tune by good players, but even then, the optimal target tuning differs from one situation to another depending no a whole host of issues. One issue is whether one is playing with other instruments that can be played with just intonation (fiddle, say) or must be played with equal temperament (guitar, say). If you are playing with the former in the key of D and are “in tune” your notes will differ from equal temperament tuning (which is what your electronic tuner might be showing) roughly as follows (where the number indicates the number of cents sharp + or flat - compared to equal temperament):
D: 0
E: +4
F#: -14
G: -2
A: +2
B: -16
Cnat: -29
C#: -10
In the list above I normalized on D, but if you chose to tune your flute based on A you would have to subtract 2 from all the numbers above. If you tuned based on G you would have to add 2, etc. So this is part of the problem: we must chose some reference point, and once we do we may not align at other reference points.
On the other hand, if you are playing with others that are playing equal temperament tuning you do not want the above deviation. But who knows what tuning (equal, or just, or some other compromise) the maker of your flute originally chose as a target. There really is no “right” answer here, just compromises.
It is the player’s job to blow the flute in tune. This is easier in the lower octave than in the third octave, so early makers of antique flutes who expected their instruments to be played extensively in the third octave (because they were used for classical music) tended to make larger compromises in the tuning of first octave notes than higher octave notes. Also, the higher octave notes stand out more when they are not in tune. But this is just one contributing factor.
Now consider what happens if the humidity and temperature in your instrument rises, say as you warm up or the room warms up. Your tuning will get sharper. You could compensate for this by pulling out the tuning slide, but this will have more impact on the higher notes (C, B A etc) than on the foot notes. If the flute maker had originally designed your flute to play with the tuning slide extended a certain amount (i.e. the flute would be “in tune with itself” with the slide extended that amount), then as you close the tuning slide less than that the notes will become progressively flatter the nearer the foot they are. So, now if you find yourself playing in a cool room, and close your slide to keep your A at 440 hz, your D will be flat. This would be the case even if the flute was “perfectly in tune” with itself (what ever that means) at a warmer temperature.
Then of course you have to factor in that different players blow sharp or flat compared to one another, and so have the slide extended to different degrees. This means that a flute that is in tune for one player at a certain temperature and humidity will not be in tune for another.
So, to cut a really long post less long, its important to train your ear so that you can hear what it means to be in tune with whoever you are playing with, then you need to be able to lip the various notes on your flute into tune at various different tuning slide extensions depending on the atmospheric conditions. The amount of adaptation you need to apply to each note will vary from one setting to another regardless of the flute. So, that is the real challenge we all struggle with! 
Jon