diff --git a/lisp/progmodes/project.el b/lisp/progmodes/project.el
index 7cdaba9c07..d7d1740cfb 100644
--- a/lisp/progmodes/project.el
+++ b/lisp/progmodes/project.el
@@ -610,6 +610,7 @@ project--vc-list-files
   (pcase backend
     (`Git
      (let* ((default-directory (expand-file-name (file-name-as-directory dir)))
+            (abbr-dd (abbreviate-file-name default-directory))
             (args '("-z"))
             (vc-git-use-literal-pathspecs nil)
             (include-untracked (project--value-in-dir
@@ -647,7 +648,7 @@ project--vc-list-files
                                    extra-ignores)))))
        (setq files
              (mapcar
-              (lambda (file) (concat default-directory file))
+              (lambda (file) (concat abbr-dd file))
               (split-string
                (apply #'vc-git--run-command-string nil "ls-files" args)
                "\0" t)))
@@ -670,6 +671,7 @@ project--vc-list-files
        (delete-consecutive-dups files)))
     (`Hg
      (let* ((default-directory (expand-file-name (file-name-as-directory dir)))
+            (abbr-dd (abbreviate-file-name default-directory))
             (include-untracked (project--value-in-dir
                                 'project-vc-include-untracked
                                 dir))
@@ -685,7 +687,7 @@ project--vc-list-files
        (with-temp-buffer
          (apply #'vc-hg-command t 0 "." "status" args)
          (mapcar
-          (lambda (s) (concat default-directory s))
+          (lambda (s) (concat abbr-dd s))
           (split-string (buffer-string) "\0" t)))))))
 
 (defun project--vc-merge-submodules-p (dir)
@@ -1042,11 +1044,8 @@ project--read-file-cpd-relative
                     (project--completing-read-strict prompt
                                                      new-collection
                                                      predicate
-                                                     hist mb-default)))
-         (absname (expand-file-name relname common-parent-directory)))
-    (when (and hist history-add-new-input)
-      (add-to-history hist (abbreviate-file-name absname)))
-    absname))
+                                                     hist mb-default))))
+    (expand-file-name relname common-parent-directory)))
 
 (defun project--read-file-absolute (prompt
                                     all-files &optional predicate
@@ -1076,9 +1075,16 @@ project-find-file-in
                dirs)
             (project-files project dirs)))
          (completion-ignore-case read-file-name-completion-ignore-case)
-         (file (funcall project-read-file-name-function
-                        "Find file" all-files nil 'file-name-history
-                        suggested-filename)))
+         (file
+          (let ((file-name-history (seq-filter
+                                    (lambda (s) (member s all-files))
+                                    file-name-history))
+                (history-add-new-input nil))
+            (funcall project-read-file-name-function
+                     "Find file" all-files nil 'file-name-history
+                     suggested-filename))))
+    (when history-add-new-input
+      (add-to-history 'file-name-history (abbreviate-file-name file)))
     (if (string= file "")
         (user-error "You didn't specify the file")
       (find-file file))))