diff --git a/src/globus_cli/termio/printers/folded_table_printer.py b/src/globus_cli/termio/printers/folded_table_printer.py
index cf77a0e53..4fc80a8e0 100644
--- a/src/globus_cli/termio/printers/folded_table_printer.py
+++ b/src/globus_cli/termio/printers/folded_table_printer.py
@@ -180,7 +180,22 @@ def content_rows(self) -> tuple[Row, ...]:
         return self.rows[1:]
 
     def fits_in_width(self, width: int) -> bool:
-        return all(x.min_rendered_width <= width for x in self.rows)
+        return self.calculate_width() <= width
+
+    def calculate_width(self) -> int:
+        """
+        For each column, find the row where that column is the max width.
+        Sum those widths + the width of the separators (3 * (ncols-1))
+        """
+        max_widths = []
+        for idx in range(self.num_columns):
+            max_widths.append(max(row.column_widths[idx] for row in self.rows))
+
+        decoration_length = 0
+        if self.folded:
+            decoration_length = 4
+
+        return sum(max_widths) + (3 * (self.num_columns - 1)) + decoration_length
 
     def fold_rows(self, n: int) -> RowTable:
         """Produce a new table with folded rows."""
@@ -247,13 +262,6 @@ def _split_level(
     def is_folded(self) -> bool:
         return len(self.grid) > 1
 
-    @functools.cached_property
-    def min_rendered_width(self) -> int:
-        decoration_length = 0
-        if self.is_folded:
-            decoration_length = 4
-        return sum(self.column_widths) + (3 * (self.num_cols - 1)) + decoration_length
-
     @functools.cached_property
     def num_cols(self) -> int:
         return max(0, *(len(subrow) for subrow in self.grid))
diff --git a/tests/unit/termio/printer/test_folded_table_printer.py b/tests/unit/termio/printer/test_folded_table_printer.py
index e9a48d3f7..1c54ae4bb 100644
--- a/tests/unit/termio/printer/test_folded_table_printer.py
+++ b/tests/unit/termio/printer/test_folded_table_printer.py
@@ -4,7 +4,7 @@
 
 from globus_cli.termio import Field
 from globus_cli.termio.printers import FoldedTablePrinter
-from globus_cli.termio.printers.folded_table_printer import Row
+from globus_cli.termio.printers.folded_table_printer import Row, RowTable
 
 
 @pytest.mark.parametrize(
@@ -197,3 +197,19 @@ def test_row_folding_with_remainder():
         ("2", "5"),
         ("3",),
     )
+
+
+def test_row_table_width_computation_is_pessimal():
+    """
+    Given a table with lopsided rows, such that each row could fit in a narrow width,
+    but when column-aligned they are wider, the table should find the width based on
+    the justification of text.
+    """
+    row1 = Row((("a" * 1000, "b"),))
+    row2 = Row((("c", "d" * 1000),))
+
+    table = RowTable((row1, row2))
+
+    # it should be the max width for each column (1000) + the width of separators (in
+    # this case, 3 for the center divider)
+    assert table.calculate_width() == 2003