The tryptophans of integral membrane proteins have been suggested to play specific roles as "interfacial anchors", based on their preference for a location near the lipid head groups. Still, the underlying mechanism behind this behavior remains unclear. NMR experiments can provide an important tool to study this interaction in an actual bilayer environment. Here solid-state deuterium nuclear magnetic resonance was used to study the tryptophans in membrane-spanning model peptides from the WALP family (acetyl-GWW(LA)nWWA-ethanolamide with n = 5 and 6.5) in samples of mechanically aligned dimyristoylphosphatidylcholine (DMPC) bilayers. The data indicate that the tryptophans near the C-terminal end of the peptide display a significantly different behavior from those near the N-terminus. This is reflected prominently in a large difference in the motion experienced by the indoles at either end of the peptide, highlighting the directionality of the helix. Nevertheless, our observations indicate high levels of motional freedom for all tryptophans in these membrane spanning domains that exceed the dynamics for the helix itself. These observations signify that steric and dynamic features of the polypeptide context modulate the tryptophan anchoring in the membrane interface. Measurements of WALP19 in the ether-linked DMPC analogue ditetradecylphosphatidylcholine (missing the lipid carbonyls) show very similar Trp dynamics and suggest similar orientations for some or all of the tryptophans. This suggests that the lipid acyl chain carbonyls play at most a minor role in the anchoring interaction between these Trp residues and the DMPC interfacial region.