diff --git a/tests/repository_simulator.py b/tests/repository_simulator.py
index 637ba42a54..d0c50bc424 100644
--- a/tests/repository_simulator.py
+++ b/tests/repository_simulator.py
@@ -45,6 +45,7 @@
 from __future__ import annotations
 
 import datetime
+import hashlib
 import logging
 import os
 import tempfile
@@ -52,7 +53,6 @@
 from typing import TYPE_CHECKING
 from urllib import parse
 
-import securesystemslib.hash as sslib_hash
 from securesystemslib.signer import CryptoSigner, Signer
 
 from tuf.api.exceptions import DownloadHTTPError
@@ -80,6 +80,8 @@
 
 SPEC_VER = ".".join(SPECIFICATION_VERSION)
 
+_HASH_ALGORITHM = "sha256"
+
 
 @dataclass
 class FetchTracker:
@@ -292,9 +294,9 @@ def _compute_hashes_and_length(
         self, role: str
     ) -> tuple[dict[str, str], int]:
         data = self.fetch_metadata(role)
-        digest_object = sslib_hash.digest(sslib_hash.DEFAULT_HASH_ALGORITHM)
+        digest_object = hashlib.new(_HASH_ALGORITHM)
         digest_object.update(data)
-        hashes = {sslib_hash.DEFAULT_HASH_ALGORITHM: digest_object.hexdigest()}
+        hashes = {_HASH_ALGORITHM: digest_object.hexdigest()}
         return hashes, len(data)
 
     def update_timestamp(self) -> None:
diff --git a/tests/test_api.py b/tests/test_api.py
index 7b80d36041..8006cd48e7 100644
--- a/tests/test_api.py
+++ b/tests/test_api.py
@@ -17,7 +17,6 @@
 from typing import ClassVar
 
 from securesystemslib import exceptions as sslib_exceptions
-from securesystemslib import hash as sslib_hash
 from securesystemslib.signer import (
     CryptoSigner,
     Key,
@@ -896,6 +895,12 @@ def test_length_and_hash_validation(self) -> None:
             # test with data as bytes
             snapshot_metafile.verify_length_and_hashes(data)
 
+            # test with custom blake algorithm
+            snapshot_metafile.hashes = {
+                "blake2b-256": "963a3c31aad8e2a91cfc603fdba12555e48dd0312674ac48cce2c19c243236a1"
+            }
+            snapshot_metafile.verify_length_and_hashes(data)
+
             # test exceptions
             expected_length = snapshot_metafile.length
             snapshot_metafile.length = 2345
@@ -958,9 +963,7 @@ def test_targetfile_from_file(self) -> None:
         # Test with a non-existing file
         file_path = os.path.join(self.repo_dir, Targets.type, "file123.txt")
         with self.assertRaises(FileNotFoundError):
-            TargetFile.from_file(
-                file_path, file_path, [sslib_hash.DEFAULT_HASH_ALGORITHM]
-            )
+            TargetFile.from_file(file_path, file_path, ["sha256"])
 
         # Test with an unsupported algorithm
         file_path = os.path.join(self.repo_dir, Targets.type, "file1.txt")
@@ -990,6 +993,12 @@ def test_targetfile_from_data(self) -> None:
         targetfile_from_data = TargetFile.from_data(target_file_path, data)
         targetfile_from_data.verify_length_and_hashes(data)
 
+        # Test with custom blake hash algorithm
+        targetfile_from_data = TargetFile.from_data(
+            target_file_path, data, ["blake2b-256"]
+        )
+        targetfile_from_data.verify_length_and_hashes(data)
+
     def test_metafile_from_data(self) -> None:
         data = b"Inline test content"
 
@@ -1013,6 +1022,10 @@ def test_metafile_from_data(self) -> None:
             ),
         )
 
+        # Test with custom blake hash algorithm
+        metafile = MetaFile.from_data(1, data, ["blake2b-256"])
+        metafile.verify_length_and_hashes(data)
+
     def test_targetfile_get_prefixed_paths(self) -> None:
         target = TargetFile(100, {"sha256": "abc", "md5": "def"}, "a/b/f.ext")
         self.assertEqual(
diff --git a/tuf/api/_payload.py b/tuf/api/_payload.py
index 56852082ea..89fcbfe812 100644
--- a/tuf/api/_payload.py
+++ b/tuf/api/_payload.py
@@ -8,8 +8,10 @@
 
 import abc
 import fnmatch
+import hashlib
 import io
 import logging
+import sys
 from dataclasses import dataclass
 from datetime import datetime, timezone
 from typing import (
@@ -21,7 +23,6 @@
 )
 
 from securesystemslib import exceptions as sslib_exceptions
-from securesystemslib import hash as sslib_hash
 from securesystemslib.signer import Key, Signature
 
 from tuf.api.exceptions import LengthOrHashMismatchError, UnsignedMetadataError
@@ -34,6 +35,9 @@
 _TARGETS = "targets"
 _TIMESTAMP = "timestamp"
 
+_DEFAULT_HASH_ALGORITHM = "sha256"
+_BLAKE_HASH_ALGORITHM = "blake2b-256"
+
 # We aim to support SPECIFICATION_VERSION and require the input metadata
 # files to have the same major version (the first number) as ours.
 SPECIFICATION_VERSION = ["1", "0", "31"]
@@ -45,6 +49,38 @@
 T = TypeVar("T", "Root", "Timestamp", "Snapshot", "Targets")
 
 
+def _get_digest(algo: str) -> Any:  # noqa: ANN401
+    """New digest helper to support custom "blake2b-256" algo name."""
+    if algo == _BLAKE_HASH_ALGORITHM:
+        return hashlib.blake2b(digest_size=32)
+
+    return hashlib.new(algo)
+
+
+def _hash_bytes(data: bytes, algo: str) -> str:
+    """Returns hexdigest for data using algo."""
+    digest = _get_digest(algo)
+    digest.update(data)
+
+    return digest.hexdigest()
+
+
+def _hash_file(f: IO[bytes], algo: str) -> str:
+    """Returns hexdigest for file using algo."""
+    f.seek(0)
+    if sys.version_info >= (3, 11):
+        digest = hashlib.file_digest(f, lambda: _get_digest(algo))  # type: ignore[arg-type]
+
+    else:
+        # Fallback for older Pythons. Chunk size is taken from the previously
+        # used and now deprecated `securesystemslib.hash.digest_fileobject`.
+        digest = _get_digest(algo)
+        for chunk in iter(lambda: f.read(4096), b""):
+            digest.update(chunk)
+
+    return digest.hexdigest()
+
+
 class Signed(metaclass=abc.ABCMeta):
     """A base class for the signed part of TUF metadata.
 
@@ -664,24 +700,18 @@ def _verify_hashes(
         data: bytes | IO[bytes], expected_hashes: dict[str, str]
     ) -> None:
         """Verify that the hash of ``data`` matches ``expected_hashes``."""
-        is_bytes = isinstance(data, bytes)
         for algo, exp_hash in expected_hashes.items():
             try:
-                if is_bytes:
-                    digest_object = sslib_hash.digest(algo)
-                    digest_object.update(data)
+                if isinstance(data, bytes):
+                    observed_hash = _hash_bytes(data, algo)
                 else:
                     # if data is not bytes, assume it is a file object
-                    digest_object = sslib_hash.digest_fileobject(data, algo)
-            except (
-                sslib_exceptions.UnsupportedAlgorithmError,
-                sslib_exceptions.FormatError,
-            ) as e:
+                    observed_hash = _hash_file(data, algo)
+            except (ValueError, TypeError) as e:
                 raise LengthOrHashMismatchError(
                     f"Unsupported algorithm '{algo}'"
                 ) from e
 
-            observed_hash = digest_object.hexdigest()
             if observed_hash != exp_hash:
                 raise LengthOrHashMismatchError(
                     f"Observed hash {observed_hash} does not match "
@@ -731,25 +761,17 @@ def _get_length_and_hashes(
         hashes = {}
 
         if hash_algorithms is None:
-            hash_algorithms = [sslib_hash.DEFAULT_HASH_ALGORITHM]
+            hash_algorithms = [_DEFAULT_HASH_ALGORITHM]
 
         for algorithm in hash_algorithms:
             try:
                 if isinstance(data, bytes):
-                    digest_object = sslib_hash.digest(algorithm)
-                    digest_object.update(data)
+                    hashes[algorithm] = _hash_bytes(data, algorithm)
                 else:
-                    digest_object = sslib_hash.digest_fileobject(
-                        data, algorithm
-                    )
-            except (
-                sslib_exceptions.UnsupportedAlgorithmError,
-                sslib_exceptions.FormatError,
-            ) as e:
+                    hashes[algorithm] = _hash_file(data, algorithm)
+            except (ValueError, TypeError) as e:
                 raise ValueError(f"Unsupported algorithm '{algorithm}'") from e
 
-            hashes[algorithm] = digest_object.hexdigest()
-
         return (length, hashes)
 
 
@@ -832,7 +854,7 @@ def from_data(
             version: Version of the metadata file.
             data: Metadata bytes that the metafile represents.
             hash_algorithms: Hash algorithms to create the hashes with. If not
-            specified, the securesystemslib default hash algorithm is used.
+            specified, "sha256" is used.
 
         Raises:
             ValueError: The hash algorithms list contains an unsupported
@@ -1150,7 +1172,7 @@ def is_delegated_path(self, target_filepath: str) -> bool:
         if self.path_hash_prefixes is not None:
             # Calculate the hash of the filepath
             # to determine in which bin to find the target.
-            digest_object = sslib_hash.digest(algorithm="sha256")
+            digest_object = hashlib.new(name="sha256")
             digest_object.update(target_filepath.encode("utf-8"))
             target_filepath_hash = digest_object.hexdigest()
 
@@ -1269,7 +1291,7 @@ def get_role_for_target(self, target_filepath: str) -> str:
             target_filepath: URL path to a target file, relative to a base
                 targets URL.
         """
-        hasher = sslib_hash.digest(algorithm="sha256")
+        hasher = hashlib.new(name="sha256")
         hasher.update(target_filepath.encode("utf-8"))
 
         # We can't ever need more than 4 bytes (32 bits).
@@ -1542,7 +1564,7 @@ def from_file(
                 targets URL.
             local_path: Local path to target file content.
             hash_algorithms: Hash algorithms to calculate hashes with. If not
-                specified the securesystemslib default hash algorithm is used.
+                specified, "sha256" is used.
 
         Raises:
             FileNotFoundError: The file doesn't exist.
@@ -1566,7 +1588,7 @@ def from_data(
                 targets URL.
             data: Target file content.
             hash_algorithms: Hash algorithms to create the hashes with. If not
-                specified the securesystemslib default hash algorithm is used.
+                specified, "sha256" is used.
 
         Raises:
             ValueError: The hash algorithms list contains an unsupported