Protein folding in the cell, especially when nascent chains emerge from the ribosomal tunnel, is poorly understood. Here, we investigate the compaction and dynamics of ribosome-bound nascent single-domain proteins via a novel technology that combines fluorescence anisotropy decay with microviscometry. We targeted the model protein sperm whale apomyoglobin (ApoMb). Previous investigations based on fluorescence anisotropy decay alone determined that a portion of ribosome-bound apoMb forms a compact structure. This work, however, could not determine the size of the compact domain. In contrast, the combination of fluorescence anisotropy with microviscometry presented here enables identifying the size of compact nascent-chain subdomains. Our results demonstrate that the independently tumbling compact subdomain of nascent apoMb contains 56-81 amino acids and lacks residues corresponding to the two native C-terminal helices (denoted as G and H), which are necessary for fully burying the nonpolar residues in the native structure. Therefore, these C-terminal residues are not available for folding into the native structure until after ribosome-release. We propose that the G-helix residues may interact with the ribosome before translation termination, given their inability to sufficiently stabilize the nascent chain until the H-helix residues become available for intramolecular folding. According to a square-well-potential model envisioning local motions across a cone, the dynamics of the compact nascent-chain subdomain is spatially confined within a cone semi-angle of 15 degrees. This result highlights the highly geometrically constrained environment of the nascent protein within the ribosome. In summary, the combination of fluorescence anisotropy decay and microviscometry is a powerful approach to determine the size of independently tumbling compact regions. This technology is convenient because it requires only a single fluorophore, and can be applied to any complex biomolecule carrying an independently tumbling compact region.