diff --git a/Lib/_pyio.py b/Lib/_pyio.py
index 75b5ad1b1a47d2..18849b309b8605 100644
--- a/Lib/_pyio.py
+++ b/Lib/_pyio.py
@@ -242,14 +242,7 @@ def open(file, mode="r", buffering=-1, encoding=None, errors=None,
             buffering = -1
             line_buffering = True
         if buffering < 0:
-            buffering = DEFAULT_BUFFER_SIZE
-            try:
-                bs = os.fstat(raw.fileno()).st_blksize
-            except (OSError, AttributeError):
-                pass
-            else:
-                if bs > 1:
-                    buffering = bs
+            buffering = raw._blksize
         if buffering < 0:
             raise ValueError("invalid buffering size")
         if buffering == 0:
@@ -1565,19 +1558,15 @@ def __init__(self, file, mode='r', closefd=True, opener=None):
                     os.set_inheritable(fd, False)
 
             self._closefd = closefd
-            fdfstat = os.fstat(fd)
+            self._stat_atopen = os.fstat(fd)
             try:
-                if stat.S_ISDIR(fdfstat.st_mode):
+                if stat.S_ISDIR(self._stat_atopen.st_mode):
                     raise IsADirectoryError(errno.EISDIR,
                                             os.strerror(errno.EISDIR), file)
             except AttributeError:
                 # Ignore the AttributeError if stat.S_ISDIR or errno.EISDIR
                 # don't exist.
                 pass
-            self._blksize = getattr(fdfstat, 'st_blksize', 0)
-            if self._blksize <= 1:
-                self._blksize = DEFAULT_BUFFER_SIZE
-            self._estimated_size = fdfstat.st_size
 
             if _setmode:
                 # don't translate newlines (\r\n <=> \n)
@@ -1623,6 +1612,17 @@ def __repr__(self):
             return ('<%s name=%r mode=%r closefd=%r>' %
                     (class_name, name, self.mode, self._closefd))
 
+    @property
+    def _blksize(self):
+        if self._stat_atopen is None:
+            return DEFAULT_BUFFER_SIZE
+
+        blksize = getattr(self._stat_atopen, "st_blksize", 0)
+        # WASI sets blsize to 0
+        if not blksize:
+            return DEFAULT_BUFFER_SIZE
+        return blksize
+
     def _checkReadable(self):
         if not self._readable:
             raise UnsupportedOperation('File not open for reading')
@@ -1655,16 +1655,20 @@ def readall(self):
         """
         self._checkClosed()
         self._checkReadable()
-        if self._estimated_size <= 0:
+        if self._stat_atopen is None or self._stat_atopen.st_size <= 0:
             bufsize = DEFAULT_BUFFER_SIZE
         else:
-            bufsize = self._estimated_size + 1
+            # In order to detect end of file, need a read() of at least 1
+            # byte which returns size 0. Oversize the buffer by 1 byte so the
+            # I/O can be completed with two read() calls (one for all data, one
+            # for EOF) without needing to resize the buffer.
+            bufsize = self._stat_atopen.st_size + 1
 
-            if self._estimated_size > 65536:
+            if self._stat_atopen.st_size > 65536:
                 try:
                     pos = os.lseek(self._fd, 0, SEEK_CUR)
-                    if self._estimated_size >= pos:
-                        bufsize = self._estimated_size - pos + 1
+                    if self._stat_atopen.st_size >= pos:
+                        bufsize = self._stat_atopen.st_size - pos + 1
                 except OSError:
                     pass
 
@@ -1742,7 +1746,7 @@ def truncate(self, size=None):
         if size is None:
             size = self.tell()
         os.ftruncate(self._fd, size)
-        self._estimated_size = size
+        self._stat_atopen = None
         return size
 
     def close(self):
diff --git a/Modules/_io/fileio.c b/Modules/_io/fileio.c
index 5d9d87d6118a75..865b0e3634f3b4 100644
--- a/Modules/_io/fileio.c
+++ b/Modules/_io/fileio.c
@@ -74,8 +74,13 @@ typedef struct {
     signed int seekable : 2; /* -1 means unknown */
     unsigned int closefd : 1;
     char finalizing;
-    unsigned int blksize;
-    Py_off_t estimated_size;
+    /* Stat result which was grabbed at file open, useful for optimizing common
+       File I/O patterns to be more efficient. This is only guidance / an
+       estimate, as it is subject to Time-Of-Check to Time-Of-Use (TOCTOU)
+       issues / bugs. Both the underlying file descriptor and file may be
+       modified outside of the fileio object / Python (ex. gh-90102, GH-121941,
+       gh-109523). */
+    struct _Py_stat_struct *stat_atopen;
     PyObject *weakreflist;
     PyObject *dict;
 } fileio;
@@ -199,8 +204,7 @@ fileio_new(PyTypeObject *type, PyObject *args, PyObject *kwds)
         self->writable = 0;
         self->appending = 0;
         self->seekable = -1;
-        self->blksize = 0;
-        self->estimated_size = -1;
+        self->stat_atopen = NULL;
         self->closefd = 1;
         self->weakreflist = NULL;
     }
@@ -256,7 +260,6 @@ _io_FileIO___init___impl(fileio *self, PyObject *nameobj, const char *mode,
 #elif !defined(MS_WINDOWS)
     int *atomic_flag_works = NULL;
 #endif
-    struct _Py_stat_struct fdfstat;
     int fstat_result;
     int async_err = 0;
 
@@ -454,9 +457,13 @@ _io_FileIO___init___impl(fileio *self, PyObject *nameobj, const char *mode,
 #endif
     }
 
-    self->blksize = DEFAULT_BUFFER_SIZE;
+    self->stat_atopen = PyMem_New(struct _Py_stat_struct, 1);
+    if (self->stat_atopen == NULL) {
+        PyErr_NoMemory();
+        goto error;
+    }
     Py_BEGIN_ALLOW_THREADS
-    fstat_result = _Py_fstat_noraise(self->fd, &fdfstat);
+    fstat_result = _Py_fstat_noraise(self->fd, self->stat_atopen);
     Py_END_ALLOW_THREADS
     if (fstat_result < 0) {
         /* Tolerate fstat() errors other than EBADF.  See Issue #25717, where
@@ -471,25 +478,21 @@ _io_FileIO___init___impl(fileio *self, PyObject *nameobj, const char *mode,
 #endif
             goto error;
         }
+
+        PyMem_Free(self->stat_atopen);
+        self->stat_atopen = NULL;
     }
     else {
 #if defined(S_ISDIR) && defined(EISDIR)
         /* On Unix, open will succeed for directories.
            In Python, there should be no file objects referring to
            directories, so we need a check.  */
-        if (S_ISDIR(fdfstat.st_mode)) {
+        if (S_ISDIR(self->stat_atopen->st_mode)) {
             errno = EISDIR;
             PyErr_SetFromErrnoWithFilenameObject(PyExc_OSError, nameobj);
             goto error;
         }
 #endif /* defined(S_ISDIR) */
-#ifdef HAVE_STRUCT_STAT_ST_BLKSIZE
-        if (fdfstat.st_blksize > 1)
-            self->blksize = fdfstat.st_blksize;
-#endif /* HAVE_STRUCT_STAT_ST_BLKSIZE */
-        if (fdfstat.st_size < PY_SSIZE_T_MAX) {
-            self->estimated_size = (Py_off_t)fdfstat.st_size;
-        }
     }
 
 #if defined(MS_WINDOWS) || defined(__CYGWIN__)
@@ -521,6 +524,10 @@ _io_FileIO___init___impl(fileio *self, PyObject *nameobj, const char *mode,
         internal_close(self);
         _PyErr_ChainExceptions1(exc);
     }
+    if (self->stat_atopen != NULL) {
+        PyMem_Free(self->stat_atopen);
+        self->stat_atopen = NULL;
+    }
 
  done:
 #ifdef MS_WINDOWS
@@ -553,6 +560,10 @@ fileio_dealloc(fileio *self)
     if (_PyIOBase_finalize((PyObject *) self) < 0)
         return;
     _PyObject_GC_UNTRACK(self);
+    if (self->stat_atopen != NULL) {
+        PyMem_Free(self->stat_atopen);
+        self->stat_atopen = NULL;
+    }
     if (self->weakreflist != NULL)
         PyObject_ClearWeakRefs((PyObject *) self);
     (void)fileio_clear(self);
@@ -725,20 +736,27 @@ _io_FileIO_readall_impl(fileio *self)
         return err_closed();
     }
 
-    end = self->estimated_size;
+    if (self->stat_atopen != NULL && self->stat_atopen->st_size < _PY_READ_MAX) {
+        end = (Py_off_t)self->stat_atopen->st_size;
+    }
+    else {
+        end = -1;
+    }
     if (end <= 0) {
         /* Use a default size and resize as needed. */
         bufsize = SMALLCHUNK;
     }
     else {
-        /* This is probably a real file, so we try to allocate a
-           buffer one byte larger than the rest of the file.  If the
-           calculation is right then we should get EOF without having
-           to enlarge the buffer. */
+        /* This is probably a real file. */
         if (end > _PY_READ_MAX - 1) {
             bufsize = _PY_READ_MAX;
         }
         else {
+            /* In order to detect end of file, need a read() of at
+               least 1 byte which returns size 0. Oversize the buffer
+               by 1 byte so the I/O can be completed with two read()
+               calls (one for all data, one for EOF) without needing
+               to resize the buffer. */
             bufsize = (size_t)end + 1;
         }
 
@@ -1094,11 +1112,13 @@ _io_FileIO_truncate_impl(fileio *self, PyTypeObject *cls, PyObject *posobj)
         return NULL;
     }
 
-    /* Sometimes a large file is truncated. While estimated_size is used as a
-    estimate, that it is much larger than the actual size can result in a
-    significant over allocation and sometimes a MemoryError / running out of
-    memory. */
-    self->estimated_size = pos;
+    /* Since the file was truncated, its size at open is no longer accurate
+       as an estimate. Clear out the stat result, and rely on dynamic resize
+       code if a readall is requested. */
+    if (self->stat_atopen != NULL) {
+        PyMem_Free(self->stat_atopen);
+        self->stat_atopen = NULL;
+    }
 
     return posobj;
 }
@@ -1229,16 +1249,27 @@ get_mode(fileio *self, void *closure)
     return PyUnicode_FromString(mode_string(self));
 }
 
+static PyObject *
+get_blksize(fileio *self, void *closure)
+{
+#ifdef HAVE_STRUCT_STAT_ST_BLKSIZE
+    if (self->stat_atopen != NULL && self->stat_atopen->st_blksize > 1) {
+        return PyLong_FromLong(self->stat_atopen->st_blksize);
+    }
+#endif /* HAVE_STRUCT_STAT_ST_BLKSIZE */
+    return PyLong_FromLong(DEFAULT_BUFFER_SIZE);
+}
+
 static PyGetSetDef fileio_getsetlist[] = {
     {"closed", (getter)get_closed, NULL, "True if the file is closed"},
     {"closefd", (getter)get_closefd, NULL,
         "True if the file descriptor will be closed by close()."},
     {"mode", (getter)get_mode, NULL, "String giving the file mode"},
+    {"_blksize", (getter)get_blksize, NULL, "Stat st_blksize if available"},
     {NULL},
 };
 
 static PyMemberDef fileio_members[] = {
-    {"_blksize", Py_T_UINT, offsetof(fileio, blksize), 0},
     {"_finalizing", Py_T_BOOL, offsetof(fileio, finalizing), 0},
     {"__weaklistoffset__", Py_T_PYSSIZET, offsetof(fileio, weakreflist), Py_READONLY},
     {"__dictoffset__", Py_T_PYSSIZET, offsetof(fileio, dict), Py_READONLY},